ISSN 1413-4703 NEOTROPICAL PRIMATES
A Journal of the Neotropical Section of the IUCN/SSC Primate Specialist Group
Volume 26 Number 1 September 2020
Editors Erwin Palacios Jessica Ward Lynch Bruna Bezerra Liliana Cortés-Ortiz Júlio César Bicca-Marques Eckhard Heymann Anita Stone
News and Book Reviews Brenda Solórzano Ernesto Rodríguez-Luna PSG Chairman Russell A. Mittermeier PSG Deputy Chairman Anthony B. Rylands Christoph Schwitzer Neotropical Primates A Journal of the Neotropical Section of the IUCN/SSC Primate Specialist Group
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ISSN 1413-4703 Abbreviation: Neotrop. Primates Editors-In-Chief: Erwin Palacios, Conservación Internacional Colombia, Bogotá DC, Colombia Jessica Ward Lynch, Institute for Society and Genetics, University of California-Los Angeles, Los Angeles, CA, USA Co-editors: Bruna Bezerra, University of Louisville, Louisville, KY, USA Liliana Cortés Ortiz, Museum of Zoology, University of Michigan, Ann Arbor, MI, USA Júlio César Bicca-Marques, Pontifícia Universidade Católica do Rio Grande do Sul, Porto Alegre, Brasil Eckhard Heymann, Deutsches Primatenzentrum, Göttingen, Germany Anita Stone, California Lutheran University, Thousand Oaks, CA, USA Founding Editors Anthony B. Rylands, Global Wildlife Conservation, Austin, TX, USA Ernesto Rodríguez-Luna, Instituto de Neuroetología, Universidad Veracruzana, Xalapa, México Editorial Board Hannah M. Buchanan-Smith, University of Stirling, Stirling, Scotland, UK Carolyn M. Crockett, Regional Primate Research Center, University of Washington, Seattle, WA, USA Stephen F. Ferrari, Universidade Federal do Sergipe, Aracajú, Brazil Russell A. Mittermeier, Global Wildlife Conservation, Austin, TX, USA Marta D. Mudry, Universidad de Buenos Aires, Argentina Anthony Rylands, Global Wildlife Conservation, Austin, TX, USA Karen B. Strier, University of Wisconsin, Madison, WI, USA Maria Emília Yamamoto, Universidade Federal do Rio Grande do Norte, Natal, Brazil Primate Specialist Group Chairman: Russell A. Mittermeier Deputy Chairs: Anthony B. Rylands and Christoph Schwitzer Executive Secretary: Ella M. Outlaw Vice Chairs, Section on Great Apes: Dirck Byler and Serge Wich Vice Chair, Section on Small Apes: Susan Cheyne Vice Chairs, Section on Human-Primate Interactions: Siân Waters and Susan Cheyne Regional Vice Chairs—Neotropics Mesoamerica: Liliana Cortés-Ortiz Andean Countries: Erwin Palacios, Eckhard W. Heymann, Fanny M. Cornejo, Stella de la Torre, and Diana C. Guzmán Brazil and the Guianas: M. Cecília M. Kierulff, Fabiano Rodrigues de Melo, Maurício Talebi, and Leandro Jerusalinsky Southern Cone: Martin Kowalewski Regional Vice Chairs —Africa Rachel Ashegbofe Ikemeh, Inza Koné, David Osei, and Janette Wallis Regional Vice Chairs —Madagascar Christoph Schwitzer, Jonah Ratsimbazafy, and Steig Johnson Regional Vice Chairs — Asia China: Baoguo Li South-east Asia/Indochina:Jatna Supriatna, Arif Setiawan, Christian Roos, Benjamin M. Rawson, Ramesh Boonratana, Le Khac Quyet, and Duc Hoang Minh South Asia: Sanjay Molur and Dilip Chetry Red List Authority: Sanjay Molur, Christoph Schwitzer, and Liz Williamson Layout: Patricia Salinas Garzón, Bogotá, DC
Impreso en Colombia - Printed in Colombia por Panamericana Formas e Impresos S.A. Neotropical Primates 26(1), September 2020 1
Articles
HUMAN-MONKEY INTERACTION DYNAMICS AND THEIR DIETARY IMPACTS ON CENTRAL AMERICAN WHITE-FACED CAPUCHINS (CEBUS IMITATOR) AT MANUEL ANTONIO NATIO- NAL PARK, COSTA RICA
Meredith Schulte1, Gustavo Gutiérrez-Espeleta2 and Jessica W. Lynch1,3
1Anthropology Department, Washington State University, Pullman WA, USA, e-mail:
Abstract
Wild capuchin monkeys are highly adaptable to anthropogenic environments. We assessed how the interaction dynamics between humans and three groups of Panamanian white-faced capuchin monkeys (Cebus imitator) in Manuel Antonio National Park, the most visited national park of Costa Rica, affected the feeding behavior and diet of these animals in 2008- 2009. On average, individual monkeys acquired 2.4 human food items per focal hour during peak hours of park visitation by humans. Although human visitors directly and indirectly provisioned monkeys in the park, 71 % of monkeys’ acquisition of human food items were a result of monkey-initiated interactions (MIIs) rather than human-initiated interactions (HIIs), and adult male monkeys were the most frequent initiators (with 157 adult male MIIs in the study period, compared to 33 initiated by adult females and 84 by juveniles). Adult male monkeys were also the most likely to make direct contact with humans to grab food (35 of 50 direct grabs of food from humans were by adult male monkeys). Adult females acquired food from humans through HIIs at about the same rate as adult males in their group. Secondary acquisition of human food from other monkeys accounted for about one-third of all events of monkey acquisition of human food, and juvenile monkeys had higher median hourly rates than adults in their group to acquire human food through secondary acquisition. Humans frequently offered fruit when provisioning (61.4 % of provisioning events), but monkeys actively acquired fruit, meat, candy, condiments, chips, crackers and dairy items, and only 36.5 % of MIIs were to acquire fruit. Our results suggest that in parks where humans have frequent contact with capuchin monkeys, park regulations should not only prohibit direct provisioning, but require visitors not to bring food into parks. Stronger measures such as fines or park expulsion for those interacting with monkeys might be more effective, and environmental education is necessary as a strategy to inform visitors what to expect from the monkeys and how to avoid accidental provisioning.
Keywords: Ethnoprimatology, tourism, anthropogenic diet, Cebus capucinus, gracile capuchin monkeys
Resumen
Los monos capuchinos silvestres son altamente adaptables a los ambientes antropogénicos. Evaluamos cómo la dinámica de interacción entre los humanos y tres grupos de monos capuchinos cariblancos panameños (Cebus imitator) en el Parque Nacional Manuel Antonio, el parque nacional más visitado de Costa Rica, afectó el comportamiento alimentario y la dieta de estos animales en 2008-2009. En promedio, los monos individuales adquirieron 2.4 alimentos de humanos por hora focal durante las horas pico de la visita de humanos al parque. Aunque los visitantes humanos aprovisionaron directa e in- directamente a los monos en el parque, el 71 % de la adquisición de ítems alimentarios de humanos por parte de los monos fue el resultado de interacciones iniciadas por los monos (MII) más que de interacciones iniciadas por los humanos (HII), y los monos machos adultos fueron los iniciadores más frecuentes (con 157 MII machos adultos en el período de estudio, en comparación con 33 iniciados por hembras adultas y 84 por juveniles). Los monos machos adultos fueron también los que más probabilidades tenían de entrar en contacto directo con los seres humanos para tomar alimentos (35 de las 50 tomas directas de alimentos de los seres humanos fueron realizadas por monos machos adultos). Las hembras adultas adquirieron comida de los humanos a través de las HIIs en aproximadamente la misma proporción que los machos adultos de su grupo. La adquisición secundaria de alimentos de otros monos representó alrededor de un tercio de todos los casos de adquisición de alimentos de humanos por parte de los monos, y los monos jóvenes tuvieron tasas horarias medias más altas que los adul- tos de su grupo para adquirir alimentos de humanos a través de la adquisición secundaria. Los humanos frecuentemente ofrecían fruta al aprovisionarles (61,4 % de los eventos de aprovisionamiento), pero los monos adquirían activamente fruta, 2 Neotropical Primates 26(1), September 2020 carne, dulces, condimentos, patatas fritas, galletas y productos lácteos, y sólo el 36,5 % de los MII fueron para adquirir fruta. Nuestros resultados sugieren que en los parques donde los humanos tienen contacto frecuente con los monos capuchinos, las regulaciones de los parques no sólo deberían prohibir el aprovisionamiento directo, sino también exigir a los visitantes que no traigan comida a los parques. Medidas más estrictas, como multas o expulsión del parque para quienes interactúen con monos, podrían ser más eficaces, y la educación ambiental es necesaria como unaestrategia para informar a los visitantes sobre lo que deben esperar de los monos y cómo evitar el aprovisionamiento accidental.
Palabras Clave: Etnoprimatología, turismo, dieta antropogénica, Cebus capucinus, monos capuchinos gráciles
Introduction While there is an increasing amount of research on the impact of anthropogenic disturbances on primate diet and Capuchin monkeys (Cebus and Sapajus) are found through- behavior, many studies of provisioned, semi-provisioned, out most of Central and South America. They are highly human-commensal and human-sympatric primates define adaptable to anthropogenic environments and populations the categories of primate overlap and interaction in di- can persist alongside humans. As monkeys become more verse ways (Sabbatini et al., 2006, 2008; McKinney, 2011; habituated to human food through mechanisms such as Campbell, 2013). A bidirectional approach to categorizing crop-foraging or provisioning by humans in parks, hu- inter-primate interactions adds additional granularity to man-monkey conflict can escalate due to the combination our understanding of the complex motivations and vari- of increased human presence and increasingly habituated ations in the way that human and non-human primates monkeys’ bold and direct foraging for human food, togeth- engage with each other around food resources in a natural er putting both species at risk for injury and disease trans- area. In order to understand the human-monkey dynamics mission, as well as for diet-related health consequences in of food transfer at MANP, we collected data on human-in- monkeys. itiated versus monkey-initiated interactions.
At the time of our study, in the late 2000s, Costa Rica was Human-initiated interactions (HIIs) involve humans se- home to a flourishing ecotourism industry, associated with lecting food for the monkeys to consume based on previous increased development and habitat fragmentation around impressions about the diets of “monkeys” as well as what primate habitats (Broadbent et al., 2012). Central Ameri- is available to feed the monkeys, while monkey-initiated can white-faced capuchin monkeys (Cebus imitator) expe- interactions (MIIs) involve capuchin individuals making rienced intense contact with humans and access to human diet choices based on the availability of human and natural food at Manuel Antonio National Park (MANP). Tourist food items, as well as their own behavioral ecology and diet groups brought large amounts of food into the park to con- preferences. A study of black capuchins (Sapajus nigritus) sume at the beach or picnic tables, so capuchins had access in Brazil showed that most interactions between humans to a wide variety of human foods in addition to their nat- and monkeys were HIIs (Fahy, 2013). In contrast in Curú ural diet. Previous studies about capuchin use of human Wildlife Refuge, Costa Rica, nearly all of the interactions resources found they will consume diverse human foods, that white-faced capuchin monkeys had with humans were from fruit to cooked foods, condiments, sweets and dairy MIIs (McKinney, 2014). products (Sabbatini et al., 2006, 2008; McKinney, 2011; Campbell, 2013). At MANP, Kaufman (2014) calculated Sabbatini and colleagues (2006) performed a survey of vis- that already in 1998, a capuchin group with high expo- itors at a national park in Brazil where bearded capuchin sure to human visitors spent 46 % of its feeding time eating monkeys (Sapajus libidinosus) utilized human foods. From human-resourced foods. However, Kaufman (2014) also a total of 300 respondents, 64.7 % thought capuchin mon- noted that capuchins got much of their human food by keys had strictly vegetarian diets (Sabbatini et al., 2016). actively searching through garbage and grabbing food from Additionally, when respondents were given a list of poten- picnic tables or out of backpacks, rather than from provi- tial foods for capuchins and asked to select those that capu- sioning initiated by humans. chins consume, fruit was the most common food category chosen (45 %), followed by leaves (28 %; Sabbatini et al., Our study examined which particular human-possessed 2016). In another study of Sapajus sp. in a park in the food resources were acquired by three capuchin groups in urban matrix of Foz de Iguaçu, respondents who visited MANP in 2008-2009, as well as how often and through the park reported that they gave the monkeys fruits or cul- what means. We were particularly interested to understand tivated items over 90 % of the time, rather than processed whether monkeys most often initiated interactions involv- foods, although respondents also mentioned that other ing food with humans, or if it was humans that initiated people gave a somewhat higher percentage of processed provisioning of the monkeys. We also aimed to determine foods, with fruit still as the majority (Suzin, 2015). These what percentage of food-related human-monkey interac- findings led to our hypothesis that HIIs would involve fruit tions involved physical contact. at significantly higher rates than other foods. Neotropical Primates 26(1), September 2020 3
While capuchin diets do contain a high percentage of fruit, (ii) frequency of HIIs compared to MIIs, and whether they also contain much more protein and fat than the diets interactions included direct or indirect contact between of frugivorous and folivorous primates, due to capuchins’ monkeys and humans; (iii) the influence of age, sex and consumption of insects and vertebrate prey (Hladik et al., group categories on the frequency of interactions and the 1971; Fragaszy et al., 2004). We predicted that human proportion of interaction types. foods with higher protein and fat content would be ob- tained more frequently by MIIs than by HIIs, as capuchins Methods are likely to prefer these foods while human visitors to the park are unlikely to consider them potential food for Study site monkeys. This study was carried out during a 15-month period (Feb- ruary-August 2008 and January-August 2009) in MANP, Capuchin monkey sex, age, and group characteristics all Puntarenas province, Central Pacific coast, Costa Rica (Ta- may affect the frequency and type of acquisition of human ble 1). This park is not only Costa Rica’s smallest national food. Studies of white-faced capuchin foraging behavior park in terms of the land area (1,625 terrestrial ha according suggest that adult male capuchin monkeys may show high- to SINAC, Sistema Nacional de Areas de Conservación, in er rates of MII acquisition behaviors as well as a higher Costa Rica), but it is also the most heavily visited national rate of direct contact interactions with humans compared park in Costa Rica (ICT, 2017), and at the time of the to adult capuchin females. At Santa Rosa National Park, study was receiving between 400 to 1000, or more, human Costa Rica, adult male Cebus imitator displayed foraging visitors per day; in 2011, MANP had over 300,000 visi- patterns that involved more opportunistic and higher-risk tors (ICT, 2017) and by 2018 this had increased to over foraging strategies compared to adult females (Rose, 1994). 500,000 visitors annually (ICT, 2017). MANP is home to Adult males have reduced vulnerability to predators com- howler monkeys Alouatta palliata, squirrel monkeys Saim- pared to female capuchins, due to significant sexual dimor- iri oerstedii citrinellus, and white-faced capuchin monkeys phism (Rose, 1994). Direct contact interactions are high Cebus imitator (sensu Rylands et al., 2013; formerly called risk interactions for monkeys as they involve extreme prox- Cebus capucinus or Cebus capucinus imitator), and many imity to humans, a potential predator and disease carrier. tourists visit this park to see these primates, although ac- In areas with low human impact, female capuchins rely on cording to a survey of visitors, primates are not the main a low-risk, stable diet consisting of foraging behaviors that draw, and could in fact be detractors from visiting the park limit exposure to predators and spend less time than males due to negative monkey-human interactions (Kaufman, on the ground (Rose, 1994). A study of Cebus imitator in 2014). Cahuita National Park in Costa Rica where monkeys have access to human food showed that 100 % of monkey-initi- Capuchin study groups ated human food acquisitions were by adult males, and that We collected behavioral data on three Cebus imitator all of these MIIs were agonistic (Campbell, 2013). groups exposed to varying levels of interaction with hu- mans (Table 1). The high-interaction group HI was com- Juvenile capuchins may be more likely to obtain human posed of 15 individuals that had near daily high-proximity resources via secondary acquisition than adults, because and food-related interactions with hundreds of national juveniles often show more interest in other monkeys’ food and international visitors. The foraging area of HI included than adults do (Visalberghi et al., 1998), with the major- a mangrove lagoon, wet tropical forest, the volunteer bunk ity of the food interest directed towards adult capuchins house and park ranger house and the two most popular rather than other juveniles (Fragaszy et al., 2004; Agostini beaches in the park (Manuel Antonio and Playa Dos). Fa- and Visalberghi, 2005). Juvenile capuchins exhibit greater cilities included a large picnic area, benches, individual pic- levels of begging and receive more food via tolerated food nic tables outside of the picnic area, and trash cans. The HI transfer than adults (Perry and Rose, 1994). group spent several hours almost every day along Manuel Antonio Beach, the picnic areas, and the beach trail, which Monkeys’ proactive human food acquisition behavior may were often occupied by hundreds of humans. vary based on amount of exposure to humans, with capu- chin groups that range most often in areas with high hu- The low-interaction groups L1 and L2 were composed of man presence more likely to actively acquire food. Here 12 and 15 individuals, respectively (Table 1); they each had we compare human-resourced food acquisition rates for occasional food-related interactions with smaller numbers three different groups of capuchin monkeys with differ- of visitors. The foraging area of L1 included a hilly pen- ent degrees of exposure to humans. The aim of this study insula at the end of the two aforementioned beaches and was to investigate the influence of human presence and their steep cliffs, and a loop trail around the perimeter of food-provisioning on the feeding behavior of capuchins the peninsula. There were no trash cans or picnic tables in in MANP. Specifically, we studied the behavior of three the L1 territory. The ranging area of L2 included part of capuchin groups with different levels of interaction with the mangrove lagoon, an extensive wet tropical forest away MANP’s visitors to assess: (i) the types of human-capuchin from hiking trails and development, as well as the main interactions observed related to human food acquisition, 4 Neotropical Primates 26(1), September 2020 trail into the park, two side trails, the houses of volunteers Monkey-Initiated Interactions (MIIs) and park rangers, and a small side beach often populated by Direct Grab: the taking of human resources directly from visitors. There were no picnic tables or trash cans in the ter- a person or from a bag/object being held or worn by a per- ritory of L2, but this group occasionally visited the Manuel son. This included grabbing food items out of a person’s Antonio beach into HI territory with access to trash cans. hand, grabbing plastic bags containing food out of a person’s hand, charging a person with a threat face until a food item Table 1. Capuchin monkey study group compositions by age-sex was dropped due to fear and then collecting the food item, classes for focal animal sampling at MANP. Infants were not in- jumping on a backpack that was being worn, or otherwise cluded as focal subjects and so not included here. directly removing a human resource from a person who was not offering the food item to the monkey at that time. Adult Males Adult Females Juveniles Indirect Grab: HI 4 3 8 the taking of human resources from a per- son when the resources were not in the person’s direct pos- L1 3 3 6 session. This included taking items from unattended back- L2 6 4 5 packs or off of unattended towels, or from tables when the food was not in someone’s personal possession. This also Capuchins were identified individually using facial fea- included grabbing food items out of trash bags on some- tures, hair color and length, scars, birthmarks, and body one’s towel. To be classified as an indirect grab, it needed to size. Using body size, genital traits, and behavior we classi- be clear that the human possessor of the food did not put fied the focal individuals in three main age-sex classes: adult the food out intentionally for the monkey to take, indi- males, adult females, and juveniles. Due to the difficulty cated by surprise or anger when the monkey obtained the in sexing juvenile capuchin monkeys (Carosi et al., 2020), food, or an attempt to discourage the monkey from eating they have not been separated by sex in our analyses. Infants or taking the food. were not included in the study as focal subjects because they did not forage on their own or interact with humans. Human-Initiated Interactions (HIIs) Direct Provisioning: the food item was given directly by Behavioral data collection a human to a monkey, through hand-to-hand or hand-to- Due to park regulations, researchers only had access to mouth provisioning. To be considered direct provisioning, MANP during ‘open hours’, 9 a.m. to 4 p.m., except for it must be clear that the human offered the food to the Mondays, when the park was closed to visitors, but the monkeys and was not simply holding food they intended researchers were allowed to visit during the same hours. to consume themselves. To be counted as direct provision- This meant that researchers would have to find the mon- ing the monkey had to accept the offered food item and key groups each day, often with help from park guides or taste, lick, bite or consume the food item. rangers. Some areas of the park were inaccessible due to the lagoon and surrounding vegetation. For this reason, data Indirect Provisioning: the food item was offered from a collection was biased towards afternoon hours. human to a monkey by the human placing it in close prox- imity to a monkey or monkeys. This often consisted of hu- Behavioral data were collected by author M.S. and field as- mans setting pieces of food on a branch, table, or trash can sistants between 9 a.m. to 4 p.m., upon finding the groups surrounded by monkeys, or throwing a food item towards for the day, using 10-min focal animal sampling at 15-min the group of monkeys. It could be distinguished from in- intervals (Altmann, 1974), collected specifically when the direct grabs in that the provisioner did not express surprise monkeys were in general proximity to humans, in order to or anger at the monkey taking the food, and there were capture human-monkey interactions. Focal animal samples attempts to encourage rather than discourage acquisition alternated through individuals in different age-sex catego- and consumption. It had to be clear that the provisioner ries. Within each focal sample ad libitum data were collect- intended for the monkeys to eat the food, and the monkey ed on all social, human interaction, and human resource had to taste, lick, try or eat the food, to be classified as acquisition behaviors. Focal samples were discarded if the provisioning. individual was not visible for more than two scan samples. Inter-observer reliability between the primary investigator Secondary Acquisition: the acquisition of human food (M.S.) and field assistants was tested by performing simul- resources by one monkey from another monkey in the taneous focal samples on the same animal and determining group. Secondary acquisition happened when one monkey a percentage of discrepancies based on total discrepancies obtained a food resource via one of the above means, and observed and total behaviors recorded. either tolerated a direct grab of pieces of the food item while still in its possession, or, discarded all or part of that resource Human resource acquisition bouts were categorized in the allowing other monkeys to indirectly scavenge the remains. following ways, based on observational data collected ad libitum during the early days of the study prior to the onset Acquisition of a food item was counted once per focal sam- systematic focal animal follow data collection: ple per food type and acquisition method. For example, Neotropical Primates 26(1), September 2020 5 being fed or grabbing a bag of cookies was counted as one Table 2. Total occurrence of capuchin food acquisition of human provisioning incident or one grab regardless of how many food in this study. Numbers indicate total number of times a cookies are eaten, or if the bag was dropped and picked monkey in a focal animal follow gained possession of a human back up by the same individual. However, a direct grab of a food resource, including direct or indirect acquisition from hu- bag of cookies followed by a direct grab of a sandwich dur- mans, as well as secondary acquisition. ing one focal sample would be considered two direct grabs. Also, direct provisioning from a bag of chips followed later Food Type HI LO1 LO2 Total (97.3 (83 (71.2 (251.5 by a direct grab of that bag of chips was considered both a hrs) hrs) hrs) hrs) direct provisioning and a direct grab. Fruits: bananas, mangos, 175 78 41 294 apples, pineapple Data Analyses Behavioral rates were calculated for each focal individual Bread: Sliced white bread, baguettes, sometimes with 50 17 18 85 by taking the total number of times the behavior occurred mayonnaise for that individual divided by the total number of focal Chips: Tortilla chips, 32 8 0 40 ‘feeding near human’ hours for that individual, calculat- potato chips, cheese puffs ed through summing 10-minute focal samples. Behavioral Meat: fried chicken, sliced 35 3 1 39 rates were calculated for age and sex classes within groups lunch meat, hot dogs and are presented as medians (Quartile 1 – Quartile 3 (In- Cookies (processed and 24 5 9 38 terquartile range)) with outliers depicted in the figures. packaged) Calculations were performed using R software. Candy: sour gummy candies, caramels, chewy 21 3 5 29 Results candies Crackers: cheese crackers, Our study included a total of 240 observation days; during soda crackers, wheat 16 2 2 20 the 156 days of quantitative data collection we collected crackers 251.5 focal ‘feeding near human’ hours across all three Condiments: mayonnaise, 18 0 1 19 groups, with 97.33 focal hours for HI, 83 focal hours for ketchup L1, and 71.17 focal hours for L2. A total of 85.83 focal Other: flavored granola hours of data were collected for adult males (AM), 81.67 bars, cut whole coconut, 11 1 7 19 for adult females (AF), and 84 for juveniles (JU). Inter-ob- unknown server reliability was confirmed at more than 95 % between Dairy: milk, cookie the principal investigator (MS) and each field assistant pri- flavored milk, American 7 0 3 10 or to including any focal follow data from that field assis- cheese tant in the study. Total items acquired 389 117 87 593 Mean overall rate of human Types of human food acquired food item acquisition per 4 1.4 1.2 2.4 Human food obtained by monkeys was classified into the focal hour following categories (Table 2): fruit, bread, chips, meat, cookies, candy, crackers, dairy, condiments, and ‘other’, which included coconuts (young green coconuts were sold outside the park for visitors to drink the coconut juice— they had a small hole sliced in the top for a straw; monkeys put their hands into the hole to scrape the meat off the in- side of the coconut). Overall, human food items were ac- quired by monkeys at a rate of 2.4 items per focal hour, but the rate of human food acquisition varied widely by capu- chin group: individuals from HI group acquired 4 human food items on average per focal hour, while L1 acquired 1.4 items and L2 acquired 1.2 items per focal hour. An overview of the different types of acquisition that occurred in the study and median individual hourly acquisition rates per group is depicted in Figure 1.
Figure 1. Median hourly rates (with quartiles and outliers) that human food was acquired by individuals during focal follows for each of the three monkey groups in the study (HI, L1, L2), separated by type of food acquisition (from left to right for each group: DG = Direct Grab, DP = Direct Provisioning, IG = Indirect Grab, IP = Indirect Provisioning, SA = Secondary Acquisition). 6 Neotropical Primates 26(1), September 2020
We expected that humans would be more likely to provi- warning behaviors. Immediately the juvenile jumped to sion monkeys with fruit compared to non-fruit items. In the ground, ran to grab the chip bag, and carried it with fact, 70 out of 114 HIIs were with fruit (61.4 %), whereas him into the trees. only 100 out of 274 MIIs were for fruit (36.5 %). The most common non-fruit food item provisioned by humans Group effects on human food acquisition to monkeys was bread (21.9 % of HII events). In contrast, The group with the greatest exposure to human visitors meat, candy, condiments, and dairy items were rarely or (HI) showed the highest number of and the highest relative never offered by humans, but all of these were taken on proportion of MIIs and direct interactions for human food many occasions by monkeys, especially in the HI group. acquisition. Acquisition of human resources by HI group was seen on 81.5 % of observation days (note that on Mon- All three monkey groups accessed both fruit and non-fruit days the park was closed to visitors; therefore, the monkeys food items from humans, but at different rates. When were acquiring food from humans on almost every day that taking into consideration both primary and secondary ac- the park was open). Food acquisition behaviors included quisition of foods by the monkeys, on average, HI group charging and threatening humans in possession of food; members acquired fruit in 3.13 bouts per focal hour, and mobbing picnic tables where food was laid out; jumping non-fruit at 1.74 bouts per focal hour; L1 accessed fruit at onto individuals’ backpacks and bags while they were being 0.90 and non-fruit at 0.40 bouts per focal hour, and L2 worn or carried; opening bags, backpacks, or other items accessed fruit at 0.38 and non-fruit at 0.86 bouts per focal on towels left unattended; opening “monkey-proof” trash hour. Some individual monkeys’ acquisition of human-re- cans to forage for scraps; picking up leftovers found on the sourced food items strongly skewed toward fruit, while ground; and being fed both by hand by visitors and indi- other monkeys ate far more non-fruit than fruit items from rectly by visitors who placed food on branches, tables, or humans, although most monkeys acquired a mix of fruit trash can lids in front of monkeys. and non-fruit resources. In contrast, acquisition of human resources by L1 group For direct contact interactions, 63 of 114 were fruit was seen on 13.2 % of observation days and for L2 group (55.3 %), whereas indirect contact interactions included on 12 %. The overlap in L1 and HI’s home ranges included fruit 107 of 274 times (39.1 %). Bread, chips, cookies and two smaller side beaches that were frequently populated by crackers were the most common non-fruit items monkeys human visitors; this area was disputed frequently in inter- acquired in indirect interactions. Secondary acquisition of group encounters between these two groups. L1 interacted human food from other capuchin monkeys was an impor- with humans when its ranging patterns crossed the trails on tant mechanism, accounting for more than one-third of all the peninsula several times per day, and occasionally when human-food acquisition events observed (206 out of 593 it traveled to one of the side beaches. On the beaches, L1 events). Secondary acquisition was biased slightly toward monkeys occasionally opened unattended backpacks and nonfruit items (89 fruit events, 117 non-fruit events). The bags, and on trails they sometimes grabbed food being preference for secondary acquisition of non-fruit items over consumed by hikers, or they were provisioned by visitors. fruit items was most marked in the HI adult females, who L2’s interactions with humans occurred primarily along the acquired 23 non-fruit items but only two fruit items from trails, with occasional provisioning and grabbing of bags other capuchin monkeys during focal follows in the study. held by tourists or food carried by tourists, and some in- cidences of jumping onto worn backpacks, particularly by Resources provisioned to the monkeys through HIIs were one young male. When L2 was on the beaches in its home always unwrapped or peeled by the humans, and offered range the monkeys sometimes explored bags, backpacks, ready to eat, while food that was grabbed by monkeys often and other items on towels that were unattended. had to be extracted from a bag, box, backpack or wrapper. Provisioning rarely involved travel on the ground, as food Sex and age differences in human food acquisition was often placed on trees, branches, tables, or directly into As overall group acquisition rates for human food were sig- the hand of the monkey. In contrast, in MIIs, monkeys nificantlydifferent from each other, we kept data separated directly approached humans, jumped onto their backs to by group in the subsequent analyses. Within each of the rummage through backpacks, or went to the ground, for three study groups, on average adult males engaged in a example to grab food from backpacks set on towels at the higher median rate of food acquisition from humans and a beach. higher proportion of MIIs to HIIs for primary human food acquisition than did adult females or juveniles (Fig. 2). The One juvenile monkey appeared to use deception to ma- majority of adult male utilization of human resources in nipulate other group members, so he could grab human MANP were the result of grabs and indirect provisioning. food from the ground. He stood on a low branch, look- Adult males for each group performed more indirect grabs ing towards a bag of cheese-flavored tortilla chips on the than adult females for that group but, did not successful- ground, while five group mates foraged on the ground ly acquire significantly more indirect provisioning items nearby. He emitted an alarm call and the other monkeys compared to adult females in their group. Within groups, jumped and ran up into the trees, performing vigilant on average adult females did not show large differences in Neotropical Primates 26(1), September 2020 7 rates of MIIs compared to HIIs, or in indirect versus direct rates of secondary acquisition of resources than their adult contact interactions. Juveniles in the HI group were more counterparts (Fig. 4). likely to initiate interactions to acquire food and, did so at a median rate of 2.46 times per focal hour, compared to juveniles in the low exposure groups, who performed suc- cessful MIIs much less frequently (LO1: 0.16; LO2: 0.30 times per focal hour).
Figure 4. Median hourly rate (with quartiles and outliers) of sec- ondary acquisition of human feeding resources, when one mon- key acquires the human resource from another monkey, by capu- chin age class and group membership.
Discussion Figure 2. Median hourly rate (with quartiles and outliers) of hu- man-initiated interactions (dark grey boxes) and monkey-initiat- Understanding how white-faced capuchins utilize human ed interactions (light grey boxes) during focal follows that led to resources is a key step in being able to manage and pre- primary monkey acquisition of human food resources, by capu- chin age, sex and group membership. vent conflict between humans and monkeys where park visitors have the opportunity to interact with wild mon- When comparing frequency of interactions with direct keys. Preventing escalating monkey-human conflicts over versus indirect contact, all age-sex classes in all groups had human-sourced food is essential not only to protect the more indirect interactions than direct interactions with integrity of the local ecosystem and health of the monkey humans. However, the median frequency of both direct population but to ensure a truly sustainable ecotourism contact and indirect contact with humans was significantly economy (Krüger, 2005; Webb and McCoy, 2014). Our higher for adult males and juveniles of the high contact results suggest that monkeys in MANP in our 2008-2009 (HI) group compared to other age-sex-group categories study period initiated the majority of interactions to access (Fig. 3). human food. While MANP park regulations at the time fo- cused exclusively on preventing tourists from provisioning the monkeys directly, our findings showed that the primary issue driving capuchin consumption of human food was capuchin access to human food, particularly for adult male and juvenile capuchins. Direct provisioning, although part of the habituation process, represents a relatively less fre- quent means by which capuchins obtain human resources. It is currently unknown whether indirect access to human food precedes monkey willingness to accept food direct- ly from humans or whether direct feeding by humans is the initial driver toward human-food seeking behaviors in monkeys. However, the indirect access to human food not intentionally facilitated by humans was a large proportion Figure 3. Median hourly rate (with quartiles and outliers) of direct contact (dark grey boxes) and indirect contact (light grey of the human food consumed by monkeys in this park, and boxes) during focal follows as the means of primary acquisition reducing that access is essential for managing the monkey of human feeding resources, by capuchin age, sex, and group consumption of human resources. We suggest that preven- membership. tion of access to human resources within parks with a high volume of visitors should be expanded beyond regulations Secondary acquisition of human food restricting direct provisioning, including using more effec- Secondary acquisition made up a substantial proportion of tive monkey-proof trash cans, limiting human food con- all human food attained in capuchin monkeys’ diet, for all sumption to an enclosed area, or restricting visitors from sex-age classes. The HI group had a higher median hourly bringing food into the parks. We also suggest that stronger rate of secondary acquisition per focal hour (1.5 acquisi- measures, such as fines or expulsion from park for those tions) compared to the other two groups (LO1 = 0.46, interacting with monkeys, might be more effective, and LO2 = 0.47). In each group juveniles had higher median that environmental education is necessary as a strategy to 8 Neotropical Primates 26(1), September 2020 inform people what to expect from the monkeys and how compared to other groups. MIIs with humans may be con- to avoid accidental provisioning. tingent on high familiarity with and desire for human re- sources, indicating enough previous exposure to a particu- In fact, in the years after our study, MANP has enforced lar resource so it no longer provokes neophobia, as well as stricter regulations, in which visitors are not allowed to a perceived value which outweighs the opportunity cost of bring food in the park, and there are spot inspections to acquisition (Visalberghi et al., 2003; Fragaszy et al., 2004; check bags for food at the entrance gate. While this has Agostini and Visalberghi, 2005). clearly improved the monkey-human interactions at the park, capuchin monkeys still patrol the beaches looking for At MANP humans preferentially offeredmonkeys more food in close contact with humans (JWL, pers. obs.); this ‘natural’ food items like fruit. However, store-bought fruit suggests that once capuchins are habituated to the possi- often has drastically higher sugar content and lower fiber bility of human food as a resource, it is hard to extinguish content than fruits in monkeys’ natural diet, such as palm their interest or habituation to humans. fruit. In addition, monkeys initiated most food interactions and preferred to acquire sugar-dense, salt-dense foods. The Adult male capuchin monkeys at MANP initiated more types of human foods consumed by the study subjects and food acquisition interactions and had higher levels of direct the high consumption rate were likely cause of acute health contact interactions than adult females in the same group. problems such as vomiting and diarrhea observed during In white-faced capuchins, males are the dispersing sex, the study. The fat, refined sugar, and sodium content of and they often disperse several times during their lifetime, foods such as cookies, candy, potato chips, fried chicken, alone or in groups (Jack and Fedigan, 2004; Fedigan and mayonnaise, and many other foods the capuchins encoun- Jack, 2012). This, in combination with males’ increasingly ter and eat have the potential to cause long-term health aggressive food acquisition techniques, suggests that when problems with reproductive consequences. In addition, habituated males from these groups disperse, they will the direct contact with humans and increased time spent continue to actively acquire human resources in their new on the ground retrieving human food may result in higher group. Juveniles obtained more of their human resources human-primate disease transmission or parasitic infections. via secondary acquisition compared to adults, suggesting a While aggression was not the primary focus of this study, route by which dispersing males, who are the most active at our observations indicated that levels of aggression between grabbing food from humans, will have a significant impact monkeys over human food resources was similar to aggres- on the diet choices of juveniles in their new groups. The sion observed over high-fat, high-protein foods in their role of social facilitation in the development of capuchin natural diet, but that human food resulted in intragroup diets means that juvenile capuchins in groups where adult aggression almost daily while high-fat, high-protein natural capuchins regularly consume human foods will learn to foods were consumed much less frequently. rely on human foods as a standard part of their diet. This suggests a small window of time for correction and mitiga- Future studies on acquisition of human food by primates tion between the habituation and provisioning of monkeys should include data regarding all available types of human by humans and the time at which monkey populations foods at the study site as well as any incidences of humans view human foods as a central part of their standard diet. unsuccessfully offering food to monkeysin order to better differentiate between opportunistic and preferential forag- Relatedly, secondary acquisition of human-resourced food ing. Collecting focal animal data across the waking hours occurred in all age-classes and groups in our study. It is of the primates, not just during visiting hours of parks, or important to recognize that human-resourced food items when monkeys were in proximity to humans, would also do not only go to the first monkeythat acquires them; they lead to less biased estimates of human food consumption also are shared within the capuchin group, potentially af- by primates. Concurrent data collection on natural food fecting diet and health of even those group members that item consumption versus human food consumption would never become strongly habituated to close contact with hu- also help to distinguish the degree of impact human food mans. For example, adult females in the HI group were rel- had on primate diet in areas where they are exposed to hu- atively risk-averse foragers, with lower rates of primary ac- man foods. quisition of human food than adult males or juveniles, but almost all of the food that they acquired secondarily from Acknowledgments other group members was non-fruit—in other words, high sugar, high fat content with potential health implications. We are grateful for logistical support and funding from Na- tional Science Foundation IPEM-IGERT grant 0549425 Analysis of capuchin groups with different levels of in- through Washington State University (WSU); MS received teraction with humans may help researchers understand funding from WSU Graduate and Professional Student how acquisition rates change over time as human presence Association. Thanks to Brian M. Kemp, Nicole Hess, and monkey habituation increase. As expected the group Courtney Meehan, Tim Kohler, Dena Spencer-Curtis, Mi- with the highest level of contact with tourists showed a sael Chinchilla Carmona, Erik Gjesfjeld, Megan Carney, higher proportion of MIIs and direct contact interactions Chad Brock, and especially to MANP administration and Neotropical Primates 26(1), September 2020 9 park rangers, and our field assistants Karlijn Moeskops, Jack, K. and Fedigan, L. M. 2004. The Demographic and Vera Lipman, Mark Clifton, Meghan Machado, and Jo- Reproductive Context of Male Replacements in Cebus sie Chambers. All methods were approved by Washington capucinus. Behaviour 141: 755–775. State University Institutional Animal Care and Use Com- Kaufman, L. 2014. Interactions between tourists and mittee, and research was carried out under Costa Rican white-faced monkeys (Cebus capucinus) at Manuel An- Ministerio de Ambiente, Energía y Telecomunicaciones/ tonio National Park, Quepos, Costa Rica. p. 230–244. 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ANTI-PREDATOR BEHAVIOR OF COIMBRA-FILHO’S TITI MONKEYS (CALLICEBUS COIMBRAI)
João Pedro Souza-Alves1,3 and Isadora P. Fontes2
1 Postgraduate Program in Animal Biology, Department of Zoology, Federal University of Pernambuco. Av. Professor Morais Rego, 1235, Cidade Universitária, Recife - PE, Brazil, 50670-901, e-mail:
Abstract
Predation pressure has an important role in shaping the behavioral, ecological and social patterns of primates. In this study, we describe two types of anti-predator behavior performed by Coimbra-Filho’s titi monkeys (Callicebus coimbrai), and compare our reports with the anti-predator strategies adopted by other Neotropical primates. The reports were performedon a small and isolated Atlantic forest fragment (14 ha) located in a highly-fragmented landscape in north-eastern Brazil. Although the titi monkey group was systematically monitored (July/2009 - August/2012: 1,513 hours) over the years, the events were recorded ab libitum method. Four events of anti-predator behavior were reported: three were in response to a medium-sized arboreal primate, the yellow-breasted capuchin monkey (Sapajus xanthosternos), and one in response to a large bird, the turkey vulture (Cathartes aura). When in the presence of S. xanthosternos, the titi monkeys emitted a quiet alert vocalization and descended to the dense undergrowth in order to avoid predation. On the other hand, when the titi monkeys were exploiting fleshy fruiton a tree, they verified the presence of an individualof C. aura and jumped to the ground. Both types of anti-predator behavior had been previously described for Neotropical primates. The anti-predator behaviors performed by the titi monkeyscan contribute to the understanding of the adaptive processes of these poorly studied primates in fragmented habitats. Moreover, the passive behavior and the habitat characteristics may be an important aspect in the choice of strategy to be used, since the habitat pro- vided adequate refuges and allowed the titi monkeys to seek an alternative escape route.
Key Words: Atlantic Forest, Sapajus xanthosternos, Cathartes aura, anti-predator strategy
Resumo
A pressão da predação tem um papel importante nos padrões comportamentais, ecológicos e sociais dos primatas. Neste estudo, descrevemos dois tipos de comportamento anti-predadores realizados por indivíduos de um grupo de Guigó-de- -Coimbra-Filho (Callicebus coimbrai) e comparamos nossos registros com as estratégias anti-predadores adoptadas por outros primatas neotropicais. Os registros foram realizados em um pequeno e isolado fragmento de Mata Atlântica localizado em uma paisagem altamente fragmentada na região nordeste do Brasil. Embora o grupo tenha sido sistematicamente monito- rado (julho/2009 – agosto/2012: 1,513 horas) ao longo dos anos, os eventos foram registrados de forma ab libitum. Foram relatados quatro eventos de comportamento anti-predador: três foram em resposta a um primata arborícola de tamanho médio, o macaco-prego-do-peito-amarelo (Sapajus xanthosternos), e um em resposta a uma ave de grande porte, o urubu- -de-cabeça-vermelha (Cathartes aura). Quando na presença de S. xanthosternos, os guigós emitiram vocalização de alerta e desceram até o sub-bosque denso a fim de evitar a predação. Por outro lado, quando os guigós estavam consumindo frutos, eles verificaram a presença de um indivíduo de C. aura e pularam para o chão. Ambos tipos de comportamentos anti-preda- tor já tinham sido previamente descritos para primatas Neotropicais. Os comportamentos anti-predadores realizados pelos guigós podem contribuir para a compreensão dos processos adaptativos destes primatas pobremente estudados em áreas frag- mentadas. Além do mais, o comportamento passivo e as características do seu hábitat podem ser um aspecto importante na escolha de estratégia a ser utilizada, uma vez que proporcionavam refúgios adequados e permitiam que os guigós buscassem uma rota de fuga alternativa.
Palavras-chave: Mata Atlântica, Sapajus xanthosternos, Cathartes aura, estratégia anti-predador
Introduction of the presence of human observers to inhibit predation bouts, and therefore the large amount of time and energy It is extremely difficult to document predation on primate needed to obtain these reports (Isbell, 1994). However, species due to the low occurrence of events, the difficul- predation pressure has an important role in the behavio- ty in observing quick predatory attacks, the nocturnal ral, ecological and social patterns of primates (van Schaik, habits of many predators (owls and leopards), the effect 1983; Cheney and Wrangham, 1987; Stanford, 2002). Neotropical Primates 26(1), September 2020 11
This pressure results in specific behavioral responses family groups and maintain strong social structures (Fer- linked to different types of predators and prey (Ferrari, rari, 2009; Dolotovskaya et al., 2019). Owl monkeys 2009). Predators or potential predators of primates in- (Aotus) and titi monkeys (Callicebus, Cheracebus and Plec- clude hawks (Heymann, 1990; Sherman, 1991; Julli- turocebus) are Neotropical primates that possess all these ot, 1994; Gilbert, 2000; Vasquez and Heymann, 2001; features (Norconk, 2011). Titi monkeys (sensu Byrne et Defler, 2004), felids (Olmos, 1993; Novak et al., 2005; al., 2016) are small-bodied primates (ca. 2 kg) distribut- Ludwig et al., 2007), other primate species (Sampaio and ed widely across diverse habitats in South America (Bic- Ferrari, 2005), and even snakes (Heymann, 1987; Corrêa ca-Marques and Heymann, 2013). They live in small and Coutinho, 1997; Teixeira et al., 2016). In order to groups comprising a monogamous breeding pair with avoid predation, the behavioral response of primates can one to three offspring (Bicca-Marques and Heymann, vary between active (i.e., mobbing, monitoring or alarm 2013). They are primarily frugivorous, exploiting alter- calling) and passive (i.e., avoiding, hiding or fleeing) be- native food resources such as new leaves and invertebrates haviors (Ferrari, 2009). during periods of lower fruit availability (Caselli & Setz, 2011; DeLuycker, 2011; Souza-Alves et al., 2011) and Anti-predator strategies can be strongly linked to predator use low and middle forest strata (Heiduck, 2002; Chagas type (Edmunds, 1974; Table 1). Practically all predators and Ferrari, 2010). Owing to behavioral and morpholog- (or potential predators) of primates demonstrate solitary ical characteristics (shiny and cryptic pelage), titi mon- foraging behavior (Ferrari, 2009). Terrestrial predators keys have demonstrated efficient passive anti-predator such as mammalian carnivores can either engage in aston- strategies (Ferrari, 2009). ishing high-speed pursuits in open habitats or can stalk, ambush and pounce to overpower prey (Macdonald et al., Here we described two types of anti-predator behavior 2010; Wilson et al., 2013; Wilson et al., 2013). On the performed by Coimbra-Filho’s titi monkeys (Callicebus other hand, aerial predators (raptors) tend to use active coimbrai) inhabiting a small Atlantic forest fragment in search or sit-and-wait strategies to pursue and capture prey north-eastern Brazil, and we compare them to the an- (see Tables 1 and 2 in Jaksic and Carothers, 1985). Moreo- ti-predator strategies adopted by other Neotropical pri- ver, arboreal predators (primates) seem to have used a “sur- mates. Coimbra-Filho’s titi monkeys are a highly frugivo- prise attack or ambush” strategy to capture a small-bodied rous species; they live in small groups, use low and middle primate (Albuquerque et al., 2014). forest strata, inhabit disturbed sites, demonstrate an in- come breeding strategy, and use the forest floorfrequently Active anti-predator behaviors may be used to commu- (Chagas and Ferrari, 2010; Chagas and Ferrari, 2011; Sou- nicate the presence of such surprise-effect dependent za-Alves et al., 2011, Souza-Alves et al., 2019), all features predators (terrestrial predators) to conspecifics. In the that put them at a high risk of predation (Ferrari, 2009). presence of terrestrial predators, primate behavior can As such, we expected that Coimbra-Filho’s titi monkeys vary between mobbing (Brachyteles hypoxanthus: Dias and would demonstrate different anti-predator behaviors when Strier, 2002; Cacajao calvus: Bowler, 2007), ascending up facing terrestrial, arboreal and aerial potential predators liv- trees (B. hypoxanthus: Mendes, 1997), approaching and ing in fragmented habitats. mobbing (Callicebus nigrifrons: Cäsar et al., 2012), or producing alarm calls (Chiropotes utahicki: Ferrari et al., Methods and Study Site 2004). In terms of aerial predators, primates can adopt a combined active/passive anti-predation strategy aiming Our study took place in a small Atlantic forest fragment to avoid predation. When under attack from aerial pred- (14 ha) at Fazenda Trapsa (11°12’ S, 37°14’ W), located in ators, primates variously produce loud calls and descend the municipality of Itaporanga d’Ajuda, state of Sergipe, within the forest canopy (Alouatta clamitans: Miranda et north-eastern Brazil. The site isembedded in a mosaic al., 2006), hide and remain vigilant (A. palliata: Gil-da- of eight forest fragments varying in their forest structure, Costa et al., 2003; Callithrix jacchus: Bezerra and Souto, size, shape and degree of conservation (Chagas and Fer- 2008), demonstrate mobbing behaviors (Saimiri oerstedii: rari, 2011). The study site is characterized by smalltrees Boinski 1987), or display piloerection (Plecturocebus cu- (mean = 8.3 m) with basal area of 39.5 m2, high density of preus: Dolotovskaya et al., 2019). When potential arbo- lianas (940 ind/ha) and is classified as being in an early real predators are noticed, primates can flee quickly and stage of regeneration (Souza-Alves et al., 2018). The pre- hide in vine tangles (Plecturocebus cupreus: Dolotovskaya dominant botanical families are Fabaceae, Myrtaceae, and et al., 2019), or moving rapidly, produce alarm call and Sapotaceae (Souza-Alves et al., 2014). Monthly rainfall mobbing vocalizations (Callithrix jacchus: Albuquerque et level (mm) was collected at the meteorological station of al., 2014). Thus, the anti-predator strategy adopted will RPPN Caju – Embrapa Sergipe, located 1 km from the depend on the context of each predation event as well as study area. During the 11-year period from 2000-2011 the primate species involved. the annual mean of rainfall recorded there was 120.9 mm (Semarh, 2017). Köppen’s classification characterizes the Primates that display passive anti-predator behaviors regional climate as As (Tropical zone with dry summer: tend to present cryptic pelage coloration, live in small Alvares et al., 2013). 12 Neotropical Primates 26(1), September 2020
At the time of the study, the Coimbra-Filho’s titi group the adult male of the focal titi monkey group visually no- comprised four individuals, with one monogamous breed- ticed the capuchin monkeys and began moving rapidly ing pair, a juvenile and an infant (Souza-Alves, 2010). between trees in the opposite direction. The researchers The subjects were previously well-habituated to human did not hear any alarm call from this individual to alert presence (Souza-Alves and Ferrari, 2010). Observations the other members of titi group, but the other members described here were obtained during the behavioral and followed this individual to avoid interaction with the capu- ecological monitoring of this titi group through scan chin group. The titi breeding pair ran in one direction and sampling for five days per month (see Souza-Alves, 2013 lay at rest 6 m from the ground until the capuchin monkey for more details). Unusual behaviors, such as anti-pred- group had passed. In contrast, the infant titi moved in the ator behavior performed by individuals, were reported opposite direction of the titi breeding pair and eventually using an ad libitum method (Altmann, 1974). When in came close to a capuchin monkey. The infant titi sighted the presence of the predator, we recorded the time of day, a capuchin 3 m away and stopped. The capuchin monkey predator taxon, and titi monkey behavior during and af- looked at the infant and continued on his route, then the ter the encounter. Here we present data related to an- infant titi moved towards the breeding pair where they re- ti-predator strategies. mained until after the capuchin monkeys left the quadrant, at which time the titi monkeys resumed their usual activ- Results ities. The titi monkeys also left and did not return to this location until the end of the day. The Coimbra-Filho’s titi monkey focal group was observed from July 2009 to August 2012, for a total of 1,513 hours. The last anti-predator strategy event was reported in Octo- Four events of anti-predator behavior were reported; three ber 2009, at approximately 09:40 am. A turkey vulture flew of these were in response to a medium-sized arboreal pri- near three members of the Coimbra-Filho’s titi group. One mate, the yellow-breasted capuchin monkey (Sapajus xan- adult and the infant were at a height of between 7 and 9 m, thosternos), and one towards a large-sized bird, the turkey feeding on Xylopia frutescens seeds (Annonaceae). The sub- vulture (Cathartes aura). adult was at a height between 2 and 3 m feeding on young leaves of unidentified vines. Noticing the turkey vulture The first event took place in July 2009, at approximately flying over the tree canopy, the titi monkeys jumped to 6:30 am, when the Coimbra-Filho’s titi group was at one the ground, stood still for 1 to 2 min and emitted an alert of their sleeping trees (ca. 1 m), Licania littoralis (Chryso- vocalization (quiet call). The individuals looked up in an balanaceae). A group of Sapajus xanthosternos composed attempt to observe the vulture and see if it had left the area. of 18 to 19 individuals approached quickly and extreme- When on the ground, the titi monkeys were at distances ly noisily. These factors allowed the members of Coim- of between 1 and 2 m from the human observer, without bra-Filho’s titi group to leave the sleeping site quickly. showing any concern. After departure of the vulture, the The titi monkeys moved to another tree in order to facil- individuals returned to their normal activities. itate their observation of the capuchin monkeys, and one individual emitted a quiet call to alert the group. On the Discussion same day around 10:45 am, the capuchin monkeys were foraging and walking towards the titi monkey group. This Our results demonstrate that, like other Neotropical pri- advance triggered the titi monkeys to quickly and quietly mates, Coimbra-Filho’s titi monkeys respond differently descend from their current location (at 12 m height) to when threatened by an arboreal versus an aerial potential approximately 3 m, where they remained and kept silent predator (Table 1). When exposed to a potential arbore- and still. All four of the titi monkeys remained stationary al predator (Sapajus xanthosternos), the titi monkey group and quiet for 15 to 20 minutes to avoid detection before tended to descend to lower forest strata (understory), hide returning to their activities. Throughout this day, how- in vine tangles, remain still and give quiet alarms. They ever, the group of titi monkeys monitored the capuchin remained in the understory to perform all their daily activ- monkey group and sought to perform their activities with ities. Robust capuchins are known to prey on titi monkeys caution, keeping close together and scanning the area due (see Sampaio & Ferrari, 2005 – Sapajus apella) as well as to the continued presence of the capuchin monkeys. on common marmosets (see Albuquerque et al. 2014 – Sa- pajus xanthosternos). In contrast, in the presence of a po- The second event occurred on May 2011 at 12:00 pm. tential aerial predator (Cathartes aura), the titis fled to the Three members of the titi monkey group were eating fleshy forest floor in order to avoid predation. Although some fruits on the Tapirira guianensis tree (Anacardiaceae) at other studies have verified primate anti-predation behavior ~15 m height and perceived the approach of the capuchin in the presence of vultures, there are no reports of vulture monkey group. All the titi monkeys descended to the un- predation on live primates (Gleason & Norconk, 2002; derstory (ca. 3 m) and hid in the vine tangles. The third Suscke et al., 2017). event was reported on February 2010 at 10:00 am when Neotropical Primates 26(1), September 2020 13
Table 1. Overview of response of the passive anti-predator behavior from Neotropical primates.
Type of predator Species Anti-predator response Source Alouatta clamitans Descend trees Miranda et al. (2006) Alouatta palliata Hide McKinney (2009) Hide/Vigilant Gil-da-Costa et al. (2003) Brachyteles hypoxanthus Infant ran Dias and Strier (2002) Cacajao calvus Look up and alert Bowler (2007) Aerial Callicebus coimbrai Looking up and jumping down from trees Present study Callicebus nigrifrons Hide/descend trees Cäsar et al. (2012a, b) Callithrix jacchus Hide Bezerra and Souto (2008) Cebus capucinus Scan the sky/descend trees Fitchel et al. (2005), Gros-Louis et al. (2008), Digweed et al. (2005) Plecturocebus cupreus Piloerection/hide Dolotovskaya et al. (2019) Brachyteles hypoxanthus Ascend trees Mendes (1997) Callithrix jacchus Stay motionless Bezerra and Souto (2008) Cebus capucinus Ascend trees Fitchel et al. (2005), Gros-Louis et al. Terrestrial (2008), Digweed et al. (2005)
Plecturocebus cupreus Piloerection/hide Dolotovskaya et al. (2019) Plecturocebus discolor Call/hide/piloerection De Luna et al. (2010) Callicebus coimbrai Hide Present study Callithrix jacchus Alarm and mobbing calls/moving Albuquerque et al. (2014) Arboreal Plecturocebus cupreus Flee and hide Dolotovskaya et al. (2019) Plecturocebus moloch Call/agitated Sampaio and Ferrari (2005)
Both types of anti-predator behavior were previously ob- Several anti-predator strategies against aerial predators served in other titi monkeys (Callicebus nigrifrons, Plec- have been reported for Neotropical primates, including turocebus cupreus, and P. discolor) when in the presence alarm calls, freezing or taking cover instantaneously (Fer- of eagles and tayras (De Luna et al., 2010; Cäsar et al., rari, 2009). Brown howler monkeys (Alouatta guariba 2012) and capuchin monkeys (Dolotovskaya et al., 2019). clamitans) have been observed to descend to the under- When in the presence of an aerial predator, red titi monkey story and remain silent and motionless when under attack (P. cupreus) individuals have been found to emit alarm vo- from a black-hawk eagle (Spizaetus tyrannus) (Miranda et calizations, display piloerection, and move to denser parts al., 2006). An adult Plecturocebus cupreus male emitted of the tree crown (Dolotovskaya et al., 2019). On the other alarm calls and moved to a denser part of the forest in the hand, Callicebus nigrifrons individuals have been observed presence of a juvenile grey-headed kite (Leptodon cayanen- to move to protected areas and “freeze” (Cäsar et al., 2013). sis) (Dolotovskaya et al., 2019). Similarly, sakis (Pithecia aequatorialis) have been shown to give alarm calls for 10 Neotropical primates often use lower and denser forest veg- minutes and drop to lower branches due to the presence of etation in order to hide from and avoid potential arboreal an unknown bird species (De Luna et al., 2010). predators. These sites appear to be an optimal refuge cho- sen by primates. Cryptic pelage coloration and the small Escaping to the ground seems to be a common behavioral size of Coimbra-Filho’s titi monkeys has likely favored activity of Neotropical primates in the presence of a potential flight behaviors and increased their ability to hide from aerial predator. Most of species tend to descend to the lower capuchin monkeys to avoid predation. Similar passive an- forest strata with the aim of hiding. Under predation pres- ti-predator behavior has been verified for other titi monkey sure from a turkey vulture, common marmosets (Callithrix species. For example, Plecturocebus discolor in equatorial jacchus) emitted alarm vocalizations, hid under leaves, and Amazonia hid in vine tangles in more than half of its en- descended to the forest ground (Lyra-Neves et al., 2007). counters with tayras (De Luna et al., 2010), and P. cupreus Callithrix parents also transferred their infants from their hid in vine tangles to avoid encountering tayras, squirrel back to their ventral region while descending and hiding monkeys and capuchin monkeys at the Estación Biológica (Lyra-Neves et al., 2007). A novel anti-predator strategy by Quebrada Blanco, north-eastern Peruvian Amazon (Dolo- Saguinus mystax and Leontocebus fuscicollis is to fall down out tovskaya et al., 2019). of trees after observing aerial predators (Heymann, 1990). 14 Neotropical Primates 26(1), September 2020
At our study site, jumping to the ground may be a risky by Deutscher Akademischer Austausch Dienst (DAAD) escape alternative for Coimbra-Filho’s titi monkeys, due during the master course. We would also like to thank to presence of a large terrestrial predator (Puma concolor: Sr. Ary Ferreira, the owner of Fazenda Trapsa, and José Chagas et al., 2010). However, risk of being predated by Elias “Bóia” for his assistance during fieldwork. Currently, a puma – these felids present an ambush strategy – prob- JPS-A is supported by FACEPE (BFP-0149-2.05/19). We ably is lower than being predated by raptors. It is likely also are grateful to Cristiane Cäsar and Jessica W. Lynch for that the vegetation structure of the forest fragment (edge valuable comments on the initial draft of this manuscript. forest, discontinuous canopy) and the structure of the feed- ing tree (open canopy, low leaves, thin and long branches) References “forced” the titi monkeys to jump to the ground. 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NOT SO PEACEFUL: AGGRESSIVE ENCOUNTERS BETWEEN BENI TITI MONKEY (PLECTU- ROCEBUS MODESTUS) GROUPS IN BOLIVIA Jesus Martinez1,3, Pamela Carvajal1,3 and Robert Wallace1,2,3
1Wildlife Conservation Society, Casilla 3-35181 SM., San Miguel, La Paz, Bolivia, e-mail:
Abstract
We report observations of intergroup interactions from a free ranging group of the endemic and threatened Beni titi monkey (Plecturocebus modestus). Our observations over the course of one study year suggest that competition for food resources is the main reason for most observed intergroup encounters (n = 64), including aggressive interactions (n = 28). Additionally, threats to group integrity, such as potential loss of members, might promote very aggressive encounters, including three fights observed between adults of neighbouring groups. We provide new information on the intraspecific relationships for these endemic primates related to their use of space and food resources.
Key Words: Plecturocebus modestus, intergroup interactions, use of space, Beni, Bolivia.
Resumen
Damos a conocer información sobre las interacciones de un grupo libre de mono lucachi cenizo o tití del Beni (Plecturoce- bus modestus) con otros grupos vecinos. Nuestras observaciones realizadas durante un año sugieren que la competición por recurso alimenticio es la razón principal para la mayoría de los encuentres entre grupos (n = 64), incluyendo interacciones agresivas (n = 28). Adicionalmente, amenazas a la integridad de grupo, como es la potencial pérdida de integrantes, podrían promover encuentros muy agresivos tales como tres peleas observadas entre adultos de grupos vecinos. Proveemos nueva información sobre las relaciones intraespecíficas de estos primates endémicos,vinculadas a su uso del espacio y de recursos alimenticios.
Palabras Clave: Plecturocebus modestus, interacciones intergrupales, uso del espacio, Beni, Bolivia.
Introduction interactions such as territorial vocalizations, to aggressive encounters (Sugiura et al., 2000; Thompson et al., 2012). In social species, such as primates, interactions between con- Information about the degree of aggression during encoun- specific groups vary in frequency and type depending on the ters can help us gain a better understanding of how social degree of territoriality in the species (Cheney, 1987). Spe- ecology and intraspecific competition condition how pop- cies living in small groups tend to have small spatial require- ulations use or share resources. ments, promoting marked territorial behavior as groups try to maintain exclusive access to areas, as observed in distinct Titi monkeys (Callicebus, Cheracebus, Plecturocebus; Byrne Neotropical primate species (Peres, 1989). Apart from the et al., 2016) are a group of Neotropical primates, charac- relationship between the frequency of intergroup encounters terized by their emission of territorial calls which regulate and group density, intergroup encounters can occur due to: intergroup spacing and help to avoid direct interactions or a) competition for access to limited defendable resources, aggression between groups (Kinzey, 1981; Bicca-Marquez and b) the need to assess dispersal and mating possibilities in and Heymann, 2013). Nevertheless, some aggressive en- surrounding groups (Sicotte and Macintosh, 2004). counters between conspecific groups of titi monkeys have been reported, although it is not clear whether they corre- Territorial defense helps a group to ensure food availabili- spond to resource or mate defense (Robinson, 1979; 1981; ty in its home range (Peres, 1989). Nevertheless, this task Price and Piedade, 2001). In general, titi monkey home represents an energetic investment in which trade-offs are ranges are small (usually less than 30 ha) which, together more favorable for species with small home ranges, capable with their territorial and monogamous mating system, sug- of patrolling most of their territory (Sigiura et al., 2000). gests food resource competition might be the most likely Intergroup encounters related to social processes such as cause for territorial defense (Peres, 1989; Bicca-Marques mating and infant defense usually involve aggression be- and Heymann, 2013). Ecological data is not available for tween individuals (Thompsonet al., 2012). However, many titi monkey species, highlighting the need for re- the cost-benefit balance conditions the type of interaction search on this diverse primate subfamily (Bicca-Marques between groups, which can vary from relatively neutral and Heymann, 2013). 18 Neotropical Primates 26(1), September 2020
The Beni titi monkey, Plecturocebus modestus, is an Endan- We sampled the occurrence of intergroup interactions by gered Bolivian endemic found in naturally fragmented for- means of ad libitum behavioral sampling (Altmann, 1974). est habitats (Martinez and Wallace, 2010, 2016a; Wallace An ‘effective interaction’ between groups was considered et al., 2013). To gather natural history knowledge not pre- when a vocal or visual stimulus from a group promoted an viously available for this species, we conducted a behavioral immediate response in another group (vocal, movement, study, and here we report on intergroup interactions from or other). We differentiated effective interactions based one focal group, including the frequency and type of inter- on the degree of contact between individuals of distinct actions (distant, direct, and aggressive), their relative loca- groups. ‘Indirect interactions’ consisted of the exchange tion, as well as details of three fight events with individuals of territorial calls or displacements between individuals from neighboring groups. In this way, we provide valuable of distinct groups with no visual contact due to distance information for a better understanding of the mechanisms or visual barriers, such as dense vegetation. As territorial underlying intergroup relationships in Callicebinae. calls can be heard from more than 500 m, indirect interac- tions can involve both direct neighboring or more distant Methods groups. ‘Direct interactions’ were considered when indi- viduals of distinct groups interacted with visual contact, We conducted our study at San Miguel cattle ranch in distinguishing ‘aggressions’ as chasing-retreat displays and the southwestern portion of Beni Department, Bolivia ‘fights’ involving aggressive physical contact. (13°57’5.49”S, 66°50’5.07”W), in the Llanos de Moxos ecosystem where forest patches are immersed in a grass- We registered the location of our focal group during each land matrix (Hanagarth, 1993). Two groups of P. modestus interaction event by means of compass bearing and dis- were observed, but only the Maramacho group (adult pair, tance to reference points. As part of our behavioral study, one juvenile, and one infant) had three direct neighboring we registered the locations of plants consumed by the fo- groups with whom it interacted (Chontal, Sujo, and Man- cal group during the entire study. This spatial informa- gal). This group was located in the southeastern edge ofa tion was mapped using a 25 × 25 m grid overlapped on the large 65 ha forest patch, so neighboring groups were to the forest patch occupied by the focal group. Additionally, northwest of the focal group (Fig. 1). We present informa- from all occurrence sampling of group displacements and tion on this focal group, observed from July 2010 to June feeding events (Altmann, 1974), we calculated the total 2011 (dry and wet seasons) for 10 days per month for an amount of time and the feeding time spent by monkeys average of 10 hours per day. per grid cell.
Based on observation hours, we calculated the frequency of the distinct intergroup interactions observed. For ag- gressions and fights, we determined the winning group based on the behavioral context. With the frequencies and locations of the interactions, we estimated the number of intergroup interactions per cell grid. We assessed the rela- tionship between interactions and feeding behavior reflect- ed through feeding time and the number of plants per grid cell (SPSS v.24, significance level 0.05).
Results
We registered 227 effective intergroup interactions be- tween our Maramacho focal group and surrounding Figure 1. Map showing intergroup interactions in the area oc- groups from 574 cases when stimuli for interactions were cupied by our focal group Maramacho and neighboring groups detected (from 1,236 hours of observation). Most of (group names in gray circles show relative location) in rela- these effective interactions (76.65 %) occurred between tion to the amount of food plants (smallest marks). Grid cells our focal group and the Chontal group (Table 1), while (25 × 25 m) show the places occupied by our focal group during the study with shading corresponding to the relative amount interactions with other direct neighboring groups were of intergroup interactions (darker shading indicates higher less frequent (9.69 % and 1.76 % for the Sujo and Man- amount of records). Circles indicate cells with aggressive inter- gal groups, respectively). The remaining interactions actions Maramacho - Chontal (more records in darker circles). (11.69 %) were territorial call exchanges between our fo- Numbers indicate cells with occurrence of: 1) first fight obser- cal group and other more distant groups in distinct forest vation, 2) fights when adults fell from trees, 3 and 4) encounters with Sujo and Mangal groups, respectively. The inset photo is a patches. This trendwas similar for indirect interactions reference image showing the area occupied by our focal group in between groups (Table 1). relation to forest coverage. Neotropical Primates 26(1), September 2020 19
Table 1. Number of each type of intergroup interaction between our Maramacho focal group and neighboring groups. Direct neighbor- ing groups marked in bold.
Group All stimuli Effective Indirect Direct Aggression Fight interactions interactions interactions Chontal 259 174 112 62 27 3 Sujo 64 22 21 1 1 0 Pozero 104 21 21 0 0 0 Corral 39 4 4 0 0 0 Mangal 12 4 3 1 0 0 Tapao 72 1 1 0 0 0 Far OSO 14 1 1 0 0 0 Oeste 7 0 0 0 0 0 Guayabochi 1 0 0 0 0 0 Far NNO 1 0 0 0 0 0 Far NNE 1 0 0 0 0 0 574 227 163 64 28 3
Direct interactions (with visual contact between groups) struggle, both individuals lost equilibrium and fell to the occurred almost exclusively between our focal group and its ground from a height of around 7 m. A few seconds later, neighbor Chontal (n = 62), with only one direct interaction both monkeys climbed trees and returned to their respec- with each of the Sujo and Mangal groups (Table 1, Fig. 1). tive groups. No further interactions occurred and there Direct interactions took place in the northwestern part of was not a clear winner. the area occupied by our focal group, that corresponds to 9.74 % of the group home range (0.94 of 9.63 ha, Fig. 1). The second case (06/10/2011) occurred in the late after- From these interactions, we observed 27 cases of aggres- noon (17:12 h), after groups were in close proximity for sive chase-retreat encounters between our focal group and almost an hour. The Maramacho infant was moving far Chontal, with the loser group leaving the ‘conflict’ site. from the adults and was chased by the Chontal adult male, The Chontal group won the majority of these encounters instigating the fight. Similar to the previous case, the Mar- (14 vs. 11). There was only one aggressive encounter ob- amacho male charged the other male and repeated a similar served between the Maramacho and Sujo groups, which fight display with the same result of both individuals falling was won by Maramacho (Table 1). from a similar height. Again, the males retreated to their respective groups with no clear winner of this encounter. We observed three fights (aggressive body contact) between individuals of the Maramacho and Chontal groups. In the Most interactions between the Maramacho and Chontal first case (05/17/2010 at 12:00 h), both adults of our focal groups occurred during the wet season, but aggressive en- group confronted the adult male of Chontal group after counters, including the intergroup fights, took placemainly he caused the retreat of the juvenile and infant of our focal in the dry season (Table 2; from 619 and 617 hours of ob- group, apparently in an accidental way as the groups had servation in wet and dry seasons, respectively). Interactions not interacted previously in the day. During the encoun- with the Sujo neighbor group occurred mainly in the wet ter, the Maramacho adult female hit the side of the body season, but the opposite happened for the Mangal group. of the Chontal male with her hand, and immediately the Maramacho adult male approached, pilo-erecting his body The locations of intergroupinteractions between Maramacho fur. There was not any direct contact between males as the and Chontal groups had relatively high plant food source den- Chontal adult male then ran away towards his territory, sities (mean of 6.8 plants per grid cell, range: 0-16, n = 15; and this encounter was considered as a win for the Mara- Fig. 1). We found that aggressive interactions mainly took macho group. place in cells with a high amount of plant food sources (Spear- man correlation: rs (52) = 0.282, p = 0.039). Monkeys also The other two fights were separated by almost exactly one spent more time in these cells (rS (174) = 0.798, p < 0.001), and year and occurred in nearby locations (Fig. 1). In the first invested more time on feeding (rs (174) = 0.826, p < 0.001). one (06/16/2010), groups met unexpectedly when moving Nevertheless, fight events occurred in cells that did not neces- during the morning (08:28 h). Just after visual contact, sarily have the highest plant food source densities (5-9 plants the adult males of each group charged each other until they per cell). The only direct and aggressive encounter between made contact holding each other by the shoulders, appar- the Maramacho and Sujo groups occurred in a grid cell with ently trying to bite each other’s arms. As a result of the just two food plants. 20 Neotropical Primates 26(1), September 2020
Table 2. Seasonal variation in the number of interactions between our focal Maramacho group and its three direct neighboring groups.
Group Season Effective Indirect Direct Aggression Fight interactions interactions interactions
Dry 77 48 29 15 3 Chontal Wet 97 64 33 12 0 Dry 4 4 0 0 0 Sujo Wet 18 17 1 1 0 Dry 4 3 1 0 0 Mangal Wet 0 0 0 0 0
Discussion focal group during chase-retreat events, which suggests the interest of both adults to maintain food resources for Titi monkeys are well known as monogamous and territo- their benefit. Nevertheless, it could also be linked to the rial species (Kinzey, 1981; Bicca-Marquez and Heymann, monogamous social organization of titi monkeys, with the 2013). Some studies have revealed low degrees of territori- adult pair sharing most activities, including territorial de- ality related to large home ranges, consisting exclusively of fense (Kinzey, 1981). territorial calls (Cheracebus torquatus, Kinzey and Robin- son, 1983; Callicebus personatus, Price and Piedade, 2001). As food resources are not homogenously distributed, are- More direct intergroup interactions occur in species need- as with higher amounts of food should be defended more ing to defend smaller home ranges (Cheracebus lugens, vigorously, as was observed in grey-cheeked mangabeys Robinson, 1979, 1981). Compared to other titi monkey (Lophocebus albigena) and redtail monkeys (Cercopithecus species, the home range of Plecturocebus modestus (9.69 ha) ascanius; Brown, 2013). Our spatial data of intergroup in- is relatively small (Martinez and Wallace, 2016a). Thus, teractions clearly show that the areas with most direct Mar- our observations of direct intergroup interactions suggest amacho-Chontal interactions offered a higher number of our focal group needed to defend a relatively small territory plant food sources as compared to other zones. Moreover, from conspecific intruders. we found that our focal group spent most of the time in grid cells with a high amount of food plant sources. This may Determining the underlying causes of the observed inter- also explain the relative lack of interactions with other neigh- actions can help to understand intraspecific competition in boring groups that occurred in areas of low food availability. Beni titi monkeys, who already face spatial restrictions in the fragmented forests they inhabit (Cheney, 1987; Mar- In addition, even though forest fragmentation in the range tinez and Wallace, 2010; Wallace et al., 2013). In the three of P. modestus is mainly the result of natural processes observed fight events, male participation suggests mate (Hanagarth, 1993), this landscape configuration results and infant defense in order to ensure reproductive success in high food resource densities towards the center of for- (Thompson et al., 2012). This type of aggression is usually est patches due to edge effects (Rogan and Lacher, 2018). initiated by incursions of males looking for reproductive Our focal group, that inhabits a marginal zone of the forest opportunities; this can include solitary males, or males who patch, moved frequently to the central part of the patch have left their original group temporarily, as observed in to look for food. This demonstrates how these primates white-thighed colobus (Colobus vellerosus: Sicotte and Mac- assessed the cost-benefits of obtaining food over the risks of intosh, 2004). Before two of the three fights reported here, aggressive intraspecific interactions, which might be more the infant of our focal group was chased by the Chontal relevant for groups living in the marginal areas of forest adult male. This shows that infant defense may have driven patches. Increased levels of forest fragmentation amplify the most aggressive encounters observed between the Mar- edge effects and could reduce thesize of feeding sites for P. amacho and Chontal groups. modestus, which might increase aggressive encounters be- tween groups and could even affect the abundanceof this As well as reproductive opportunities, the need to ensure threatened primate species (Rogan and Lacher, 2018). access to food resources can promote active territorial de- fense and can be distinguished according to which group Reduced availability of food resources during lean periods members are involved (Sigiura et al., 2000; Sicotte and can promote their vigorous defense, but species with small Macintosh, 2004). Female active defense of food resourc- home ranges are more sensitive to intergroup encounters es is expected to ensure reproductive success, but similar and may need to defend their food resources against invad- defense can be carried out also by males as an indirect way ers even during periods of food abundance, as observed in to ensure permanence of female(s) in a group (Thompson Tana River crested mangabeys (Cercocebus galeritus; Kin- et al., 2012). In our study, a great majority of the direct naird, 1992). Our data shows the latter trend, with more interactions involved both male and female adults of the interactions between the focal Maramacho group and its Neotropical Primates 26(1), September 2020 21 neighbors during the wet season, with aggressive encoun- This is the first study about intergroup relationships of Plec- ters occurring mainly in the dry period when the youngest turocebus modestus, providing valuable knowledge to better individual of our focal group showed independence from understand how these endemic Bolivian primates use and adults. This suggests that the most frequent motivation defend food resources and retain group integrity. Although for intergroup interactions for our focal P. modestus group our data come from just one focal group, they represent might be food resource defense against individuals of other a good starting point for further detailed research on in- groups. traspecific relationships in this threatened primate within the naturally fragmented forests of southwestern Beni De- Based on our results, there seem to be two main triggers partment, Bolivia. for the distinct intergroup interactions observed between our focal group of P. modestus and its neighbors. Food Acknowledgements resources are vigorously defended, but not with so high intensity as occurs with mate or infant defense, as ob- We thank the Wildlife Conservation Society, the Gordon served in moustached tamarins (Saguinus mystax: Garber and Betty Moore Foundation, Primate Conservation Inc., et al., 1993) and Japanese macaques (Macaca fuscata: Margot Marsh Biodiversity Foundation, the BP Conser- Saito et al., 1998), showing that long-term reproductive vation Leadership Program and the Conservation Interna- success has higher priority than short-term disputes over tional Primate Action Fund for financial support. We are food. Our observations suggest that territorial calls and grateful to the National Directorate for the Protection of chase-retreat events might be a sufficient response for Biodiversity for help in acquiring necessary research permits. food resource defense, whereas infant defense is in re- We also acknowledge the collaboration of the Municipality sponse to high risks to reproductive success, making fight of Santa Rosa del Yacuma, and especially the Nogales cattle encounters worthwhile. ranches for access to the study site. Finally, we recognize the wonderful support of our field assistants Edson (Kayo) Gon- Aggressive interactions between groups can result in re- zales and Eduardo (Lalo) Fernandez, as well as Andrea Arnez duced access to areas with resources by the losing group and Leslie Morrison who helped during fieldwork. (Gordon, 1996), which could affect group permanence in the long term, as was reported for baboons (Papio cy- References nocephalus) unable to exploit food resources in a conflict area (Mackhan et al., 2012). Although the neighboring Altmann, J. 1974. Observational study of behaviour: sam- Chontal group won more of the intergroup encounters pling methods. Behaviour 49:227–265. against our focal group, the difference was not great (14 vs. Bicca-Marques, J. C., and Heymann, E. W. 2013. Ecolo- 11), and we observed our focal group using food resources gy and behavior of titi monkeys (genus Callicebus). In: in the conflict area during the entire study. Home range Evolutionary Biology and Conservation of Titis, Sakis and overlaps of up to 16.6 % was reported in groups of Cherace- Uacaris, L. M. Veiga, A. A. Barnett, S. F. Ferrari, and M. bus lugens, whose home ranges varied between 3 and 4 ha A. Norconk (eds.), pp.196-207. Cambridge University (Robinson, 1979). 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UNUSUAL BEHAVIORAL RESPONSES OF THE SOUTH AMERICAN COATI (NASUA NASUA) TO THE HOODED CAPUCHIN (SAPAJUS CAY) IN THE PARAGUAYAN UPPER PARANÁ ATLANTIC FOREST Rebecca L. Smith1, 2, Emily Briggs1, 3, 4 and Paul Smith1, 5
1 Fundación Para La Tierra, Centro IDEAL, 321, Mariscal José Félix Estigarribia, c/ Teniente Capurro, Pilar, Ñeembucú, Paraguay, e-mail:
Abstract
In eastern Paraguay, the South American coati Nasua nasua and hooded capuchin Sapajus cay are sympatric across most of their range. Both species are diurnal, arboreal, omnivorous mammals and have similar diets consisting of fleshy fruits and insects and are therefore potential competitors. In this article, we report three observations of unusual behavioral responses of coatis to the presence of hooded capuchins. On two occasions groups of coatis elected to show avoidance behavior by hiding from capuchin groups, despite the much closer proximity of human observers. On another occasion coatis and capu- chins were seen to feed side by side in a fruit tree without antagonism for over half an hour. We also review the literature to begin the process of identifying the factors that may influence the frequency and outcome of such encounters.
Key Words: Atlantic Forest, Behavior, Cebidae, Interspecific competition, Paraguay, Procyonidae
Resumen
En el oriente de Paraguay, el coatí sudamericano Nasua nasua y el capuchino encapuchado Sapajus cay son simpátricos en la mayor parte de su rango. Ambas especies son mamíferos diurnos, arbóreos y omnívoros y tienen dietas similares que con- sisten en frutos carnosos e insectos y, por lo tanto, son competidores potenciales. En este artículo, reportamos tres observa- ciones de respuestas de comportamiento inusual de los coatíes a la presencia de capuchinos encapuchados. En dos ocasiones los grupos de coatíes eligieron mostrar un comportamiento de evasión escondiéndose de los grupos de capuchinos, a pesar de la proximidad mucho más cercana de los observadores humanos. En otra ocasión se vio que los coatíes y los capuchinos se alimentaban uno al lado del otro en un árbol frutal sin antagonismo durante más de media hora. También revisamos la literatura para comenzar el proceso de identificación de los factores quepueden influir en la frecuencia y el resultado de tales encuentros.
Palabras Clave: Bosque Atlántico, Comportamiento; Cebidae, Competición interespecífica; Paraguay; Procyonidae
Introduction of Goiás, Mato Grosso, Mato Grosso do Sul and margin- ally into Rondônia) (Stallings, 1985; Lynch Alfaro et al., Interspecific interactions are an important and yet fre- 2012; Wallace, 2015). Hooded capuchins live in large quently overlooked part of wild animal ecology (Jones et multi-male, multi-female groups (Pinto, 2006; Fernandes al., 1994), and they may vary in nature depending on the Jr., 2013; Smith and Briggs, 2015), however the only in- ecological relationships between those species involved terspecies interactions that we are aware of include feeding (Resende et al., 2004; Fack et al., 2019). The most com- associations with collared peccary Pecari tajacu in the Bra- monly reported interspecific interactionsbetween primate zilian Pantanal (Tortato et al., 2014), sleeping, and some- and non-primate species include agonistic interactions times feeding, in the same area as black-and-gold howler (predator–prey and competitive interactions) and non-ag- monkeys (Alouatta caraya) in Nueva Gambach, Paraguay onistic interactions (affiliative and neutral interactions) (Rebecca L. Smith, pers. obs.) and an observation of pre- (Asensio and Gómez-Marín, 2002; Rose et al., 2003; Res- dation of a black tailed marmoset (Mico melanurus) in the ende et al., 2004; Cristóbal-Azkarate et al., 2015; Fernan- Brazilian Pantanal (Porfilio et al., 2017). In general, very dez et al., 2017). little is known about the behavioral ecology of the hooded capuchin, with very few studies, and no long-term studies, The hooded capuchin (Sapajus cay: Illiger, 1815) is found published from any part of its range (Brown and Zunino, in sympatry with the coati throughout eastern Paraguay, 1990; Smith and Briggs, 2016; Smith, 2017; Smith and south-east Bolivia, northern Argentina, and Brazil (states Payne, 2017; Smith et al., 2018; da Costa et al., 2020). 24 Neotropical Primates 26(1), September 2020
The South American coati Nasua nasua Linnaeus, 1766 is Here we provide descriptions of new observations of interac- widely distributed from Venezuela and Colombia, south tions between South American coatis and hooded capuchins to Uruguay and northern Argentina (Alves-Costa et al., from eastern Paraguay, and through reviewing the published 2004, Emmons and Helgen, 2016). Coatis are mainly literature we attempt to identify what factors may influence found in forested areas, both humid and dry, including the frequency and outcome of such encounters. in Paraguay gallery forest, Atlantic Forest, palm savan- nas, Cerradón and xeric Chaco forests (Emmons, 1990; Methods Gompper and Decker, 1998; Beisiegel, 2001; Trovati et al., 2010). They are a social procyonid, living in large groups The observations described here were obtained at two study made up of adult females and their offspring, with males sites in eastern Paraguay. Rancho Laguna Blanca (RLB) is typically being solitary (Russell, 1981; Haugaasen and Pe- an 804 ha property in San Pedro department, eastern Para- res, 2008; Hirsch, 2011). Adult males will occasionally guay, including an isolated and disturbed 243 ha fragment associate with groups of females (Hirsch, 2011), though of Upper Paraná Atlantic Forest. This fragment is home usually only one male per group (Hirsch, 2006). Coatis to two groups of hooded capuchins: O Group (18 indi- have been reported as forming feeding associations with viduals) (Smith and Briggs, 2015) and F Group (21 in- birds (Booth-Binczik et al., 2004, Beisiegel, 2007), pecca- dividuals). The population size of coatis in this fragment ries Pecari tajacu (Desbiez et al., 2010), tapirs Tapirus bair- was unknown. Encounters between the monkeys and oth- dii (Overall, 1980), and primates (Haugaasen and Peres, er mammalian species were observed occasionally. At the 2008, Desbiez et al., 2010). time we recorded our observations, the capuchins were in the process of being habituated to researcher presence. A The coati occurs in sympatry over much of its South Amer- typical response to human presence was for them to alarm ican range with several other species of capuchin monkeys call and flee. (Sapajus and Cebus species) with which feeding associations have also been reported (Resende et al., 2004, Haugaasen “Área para Parque” San Rafael is a 73,000 ha patch of near and Peres, 2008). Coatis, in common with many Neotrop- pristine Upper Paraná Atlantic Forest (BAAPA) in depart- ical primates (including capuchins), are diurnal omnivores ments Itapúa and Caazapá in the south of Paraguay. San that forage mainly on mature fruits and invertebrates (Izar, Rafael the largest remaining tract of BAAPA left in Par- 2004; Resende et al., 2004; Costa et al., 2009; Hirsch, 2009; aguay and consists of more than 50 private properties. Hirsch et al., 2013; de Almeida et al., 2018), creating poten- Nueva Gambach is the southernmost property with 15 ha tial for interaction at feeding sites (Alves-Costa et al., 2004; of forest connecting at its northern end to the rest of San Cristóbal-Azkarate et al., 2015; Fernandez et al., 2017). In Rafael. Nueva Gambach is home to four groups of hooded several publications that have commented on interactions capuchins (20-25 individuals per group) and an unknown between coati and primate species, interactions were ap- number of coatis. parently either mutualistic or commensal (Haugaasen and Peres, 2008, Desbiez et al., 2010), yet others resulted in con- Observations were obtained during daily monitoring (from flict (Fragaszy et al., 2004; Resende et al., 2004; Fack et al., 2013 to 2017 at RLB, and from 2017 to present at Nueva 2018), Gracile capuchins (genus Cebus) have even been re- Gambach) as part of the Para La Tierra Capuchin Research ported to predate coati pups (Newcomer and de Farcy, 1985; Project. Data were collected six days per week at RLB and Fedigan, 1990; Perry and Rose, 1994). Though we are un- for 15 days per month at Nueva Gambach. The capuchins aware of published reports of robust capuchins (genus Sapa- were followed for as long as possible between dawn and jus) predating coatis, they are known to consume vertebrate dusk and all social behavior was recorded using one-min- prey (Izawa, 1978; Terbourgh, 1983; Galetti, 1990; Resende ute scan sampling (Altmann, 1974), including interspecific et al., 2003; Sampiao and Ferrari, 2005; Carretero-Pinzón et interactions. al., 2008; Rebecca L. Smith, pers. obs.). Previous studies have reported that when groups of coa- Frequencies of coati-primate encounters are likely mit- tis are disturbed in the trees they come to the ground and igated by movement patterns, with most Neotropical escape on the ground (Gompper and Decker, 1998). Co- monkeys foraging in the trees and coatis usually foraging atis are hunted by people at both sites and it was not the on the ground (Hirsch et al., 2013). Capuchins addition- normal response to either approach humans, or to remain ally show a largely lineal foraging pattern in the canopy, close and keep still, in the presence of human observers. while coatis follow a more circuitous route on the ground, Normally, observer encounters with solitary individuals often visiting the same fruiting tree more than once a day or larger groups of coatis in the absence of capuchins re- (Hirsch et al., 2013). However, the existence of cross- sulted in the coatis either moving into the forest canopy site differences in foraging behavior in capuchins is well and hiding from observers or fleeing on the ground while known, even in geographically proximate populations vocalizing loudly. Retreating higher into the canopy was (Panger et al., 2002). more commonly observed for solitary individuals than for groups at both sites. Neotropical Primates 26(1), September 2020 25
Results a result of their belligerent natures, capuchin species can frequently behave aggressively towards competitors (Freese, Rancho Laguna Blanca: On 16 July 2014 at 08:14, a pre- 1978; Rose, 1997; Dias and Strier, 2000; Rose et al., 2003; sumed adult male coati (solitary) was observed while the Resende et al., 2004; Buchanan-Smith et al., 2013). The authors were following O Group (RLB: −23.829444, most commonly observed interactions between capuchins −56.294722). The coati had pushed its body underneath in two areas of São Paulo, Brazil (Sapajus spp. in Tiete Eco- a large mass of woody vines on a tree trunk approximately logical Park and Sapajus nigritus in Carlos Botelho State 1 m above the ground. The capuchin group was located Park) and coatis were attacks and threats by the capuchins 8 m laterally from the coati and between 5 to 7 m high- (Resende et al., 2004). The same study also recorded both er up in the canopy, while the human observers were ap- interspecific playing and four capuchin attacks on coa- proximately 2 m from the coati. Rather than fleeing on ti nests (though there was no definitive evidence of con- the ground (as is habitual), the coati slowly tried to move sumption of coatis by the monkeys) (Resende et al., 2004). higher into the tree, freezing whenever the alarm call of the Haugaasen and Peres (2008) however reported “Cebus monkeys could be heard. Three adult male monkeys then apella” (probably Sapajus macrocephalus Spix, 1823) in began to threaten the observers by vocalizing loudly and the Purus region of Amazonian Brazil feeding side by side breaking branches, but the coati remained completely still with coatis for prolonged periods with no interaction or and silent. Despite the closer proximity of the humans, the aggression; this was similar to what we observed between coati’s gaze remained directed towards the monkeys as they the hooded capuchins and the coatis in Nueva Gambach. vocalized, switching the gaze back to the human observers Clearly interactions between capuchins and coatis are during the pauses. The coati remained in this position for more complex than fixed interspecific antagonism or -in 11 minutes until the capuchins travelled out of sight; at difference, and many other factors may also influence the that point, the coati moved higher into the tree apparently outcome of these interactions, including, but not restrict- to increase the distance from the human observers. ed to context, age or status of individuals involved, levels of threat posed, resource availability, and environmental On 2nd September 2014 at 08:30, three adult coatis were conditions. encountered sitting silently on an exposed branch at a height of 5 m from the ground, just below the canopy of The differential response of coatis to humans in the pres- a mid-canopy tree (RLB:−23.829814, −56.296003). The ence or absence of capuchins at RLB suggests that they may coatis remained still and watched the human observers for be assessing risk in deciding how to respond. It is clear around four minutes. The coatis then shifted their gaze from the flight reaction in the absence of capuchins that eastwards through the canopy and did not return their gaze humans are viewed as a threat, yet the presence of capu- to the observers on the ground. Without vocalizing, the chins significantly alters this response. The apparent re- coatis then moved slowly and quietly into the denser leafy luctance of the Rancho Laguna Blanca animals to draw the vegetation of the tree top branches, approximately 9 m attention of the capuchins to their presence might suggest high and out of sight of the observers. Once the coatis were that interspecific reactions between the two species at this out of sight observers spotted the O Group capuchins ap- site are potentially agonistic, and the differential response proximately 50 m southeast of the tree in which the coatis to the presence of human observers when the capuchins hid, in the same direction that the coatis had been looking are also present could indicate that the coatis perceive the prior to hiding in the treetop. monkeys to represent a greater risk. However, in reality the risk being assessed is rather more complex. Nueva Gambach: On the 17th August 2017, a group of cap- uchins (around 20 individuals) was encountered feeding in a The observations in which coatis adopted a cautious re- Ficus enormis at 15:55 (−26.62128, −55.66998). Also feed- sponse to the presence of monkeys involved a small num- ing in the same tree, there was a large group of coatis (around ber of individuals, greatly outnumbered by the capuchins. 15 individuals) and a group of Paraguayan howler monkeys On the other hand, the peaceful foraging situation ob- (Alouatta caraya) (four individuals). At 16:15, an adult coa- served at Nueva Gambach involved similar-sized troops ti of undetermined sex approached an adult male capuchin of both species (~20 and ~15 individuals respectively). while he was feeding. Thecapuchin turned his back on the Previous studies have discovered that both coatis and cap- coati and continued to feed and the coati travelled past him. uchins are individually less vigilant when they are in larg- All of the animals fed in close proximity to one another with er groups than in smaller groups (Burger and Gochfeld, no obvious aggression for 31 minutes before the capuchins 1992; Burger, 2001; Di Blanco and Hirsch, 2006). Sim- and the coatis left the tree at 16:26 in opposite directions, ilar interactions between small groups of coatis and pri- the feeding patch apparently depleted. mates present in larger groups have been reported perhaps indicating that primates are most likely to respond with Discussion aggression when they outnumber the competitor (capu- chins: Fragaszy et al., 2004; Resende et al., 2004; Asensio There are conflicting published reports on interactions et al., 2007; woolly monkeys (Lagothrix flavicauda): Fack between capuchins and coatis in the wild (Table 1). As et al., 2018). 26 Neotropical Primates 26(1), September 2020
Table 1. Summary of interactions between coatis and capuchins.
Capuchin species Coati species Type of Behavior Study site Reference Interaction Sapajus cay Nasua nasua Avoidance Coati hid close to Rancho Laguna Blanca, San This study human observers until Pedro, Paraguay capuchin group had moved away Sapajus cay Nasua nasua Avoidance Stayed silent in the Rancho Laguna Blanca, San This study presence of human Pedro, Paraguay observer until capuchins had moved away Sapajus cay Nasua nasua Neutral Feeding in same tree Nueva Gambach, Itapúa, This study with no aggression Paraguay (howler monkeys also present) “Cebus apella” (Sapajus Nasua nasua Neutral Feeding in same area Purus region of Amazonian Haugaasen and macrocephalus) with no aggression Brazil Peres, 2008 Cebus capucinus Nasua narica Neutral Drinking together Santa Rosa National Park, Freese, 1978 at a waterhole with Costa Rica occasional threat from capuchins towards coatis Sapajus spp. (Tiete Ecological Nasua nasua Affiliative Playing together Tiete Ecological Park and Resende Park) & Sapajus nigritus Carlos Botelho State Park in et al., 2004 (Carlos Botelho State Park) São Paulo, Brazil Sapajus libidinosus Nasua nasua Agonistic Capuchins directed Tiete Ecological Park and Resende threats and attacks Carlos Botelho State Park in et al., 2004 towards coatis São Paulo, Brazil Cebus capucinus Nasua narica Agonistic Capuchins predating on Santa Rosa National Park/ Rose coati nestlings Lomas Barbudal, Costa et al., 2003 Rica Cebus capucinus Nasua narica Agonistic Capuchins chasing larger Santa Rosa National Park/ Rose coati pups and drowning Lomas Barbudal, Costa et al., 2003 of larger pups Rica Sapajus spp. (Tiete Ecological Nasua nasua Agonistic Nest attacks Tiete Ecological Park, São Resende Park) Paulo, Brazil et al., 2004
Resource availability may play an important role in how Though different taxa are involved in these observations, species interact. It has been hypothesized that robust cap- we suggest that it oversimplifies the complexity of interac- uchins will prey on coati nestlings under certain ecological tions of highly cognitive species such as the coati and the conditions such as food shortages for capuchins coincid- capuchin if we assume that such interactions are fixed at ing with coati birth season, high population densities or the interspecific level rather than multi-factorial, ecolog- high home range overlapping (Resende et al., 2004). Af- ically-influenced or learned (Romero and Aureli, 2008; filiative behavior between capuchins and coatis was never Hirsch et al., 2012; Gasco et al., 2016). No systematic observed at RLB, though neither was direct predation on investigation of interspecific interactions of large mammals coatis. Both capuchin groups at RLB were observed to ag- has been carried out in the Paraguayan Atlantic Forest and gressively mob other large mammals including tayra (Eira there is little information regarding the hooded capuchin barbara) (three observations), Paraguayan howler monkeys in general across its entire range. Further studies are re- (Alouatta caraya) (six observations), and puma (Puma con- quired to identify the potentially multiple and complex color) (one observation). In forest fragments competition factors that may determine such behaviors. can play a much greater role in regulating the abundance of species within different niches (Kozakiewicz, 1993). As Acknowledgments coatis and capuchins show dietary overlap (Resende et al., 2004) it may be that the capuchins in Laguna Blanca pre- We would like to thank all Para La Tierra staff, volunteers sented a greater threat to the coatis, not solely as potential and interns who have contributed to the PLT Capuchin predators but as a result of increased competition for more Project over the years. Thank you to the communities of limited resources in a poorer quality forest. Santa Barbara, Alto Vera and Pilar for making Paraguay Neotropical Primates 26(1), September 2020 27 home. Rebecca L. Smith extends particular thanks to the Carretero-Pinzón, X., Defler, T. R. and Ferrera, S. F. 2008. National Geographic Society for their support of the cap- Observation of black-capped capuchins (Cebus apella) uchin project (Grant Number: NGS-299C-18) and the feeding on an owl monkey (Aotus brumbacki) in the Co- Elphinstone Scholarship (University of Aberdeen). Rebec- lombian Llanos. Neotrop. Primates 15: 62–63. ca L. Smith and Paul Smith are grateful to the PRONII Costa, E. M. J., Mauro, R. A., and Silva, J. A. 2009. Group program of CONACyT Paraguay. Thanks to Hostettler composition and activity patterns of brown-nosed coatis S.A. and Pedro Hostettler for supporting the project and in savanna fragments, Mato Grosso do Sul, Brazil. Brazil. allowing us to work on the Estancia Nueva Gambach prop- J. Biol. 69: 985–991. erty. Thanks to Hans Hostettler and Christine Kohli de Cristóbal-Azkarate, J., Urbani, B., and Asensio, N. 2015. Hostettler for all of their support and to PRO COSARA Interactions of howler monkeys with other vertebrates: a for providing accommodation for the team. Thanks to the review. In: Howler Monkeys: Behavior, Ecology, and Conser- Estate of Don Julio Contreras for their continuing support vation, M. M. Kowalewski P. A. Garber, L. Cortés-Ortiz, of Para La Tierra. B. Urbani and D. Youlatos (eds), pp.141–164. Springer Press, New York. 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TRENDS IN THE USE OF STUDBOOKS IN CAPTIVE BREEDING PROGRAMS OF NEOTROPICAL PRIMATES María Laura Muñoz-Lora1, 2, Kárem Gómez-Cadenas1, Ana Carolina Falla3 and Iván Darío Soto-Calderón1
1Laboratorio de Genética Animal, Grupo de Investigación en Agrociencias, Biodiversidad y Territorio. Universidad de Antioquia, Calle 70 No. 52 - 21, Medellín, Antioquia, Colombia, e-mail: < [email protected]> 2 Universidad Eafit, Carrera 49 No. 7 Sur - 50, Medellín, Antioquia, Colombia. 3 Universidad de Ciencias Aplicadas y Ambientales (U.D.C.A), Calle 222 No. 55 - 37, Bogotá D.C., Colombia.
Abstract
Studbooks are databases of individual genealogical records of ex situ populations. Since they are an essential tool in man- agement and planning, we conducted a search of studbook reports to explore historical trends in breeding programs of Neo- tropical primates and implications for ex situ conservation. We accessed two databases: one made by the World Association of Zoos and Aquariums (WD) and another one compiled from academic reports and public internet records (PD). WD was comprised of 104 reports (1998-2011) from three habitat and seven non-habitat regions for 44 species. PD consisted of 222 reports for 34 species from two habitat and three non-habitat regions (1973-2019). International studbooks were more frequent in PD (82 %), whereas regional reports were more frequent in WD (55.8 %). Both databases showed that IUCN levels (LC, NT, VU, EN, CR and DD) with a larger number of species contain a larger number of species with studbooks and a larger number of studbooks. Therefore, there is a bias towards more studbooks on LC (Least Concern) species. De- spite limitations in availability and access to studbook records, our results revealed a discrepancy between regions where in situ conservation and ex situ conservation actions have been made. This underscores the need for international cooperation to strengthen conservation efforts, build infrastructure, increase effective population sizes and ultimately establish viable populations. Finally, we advise assessing opportunities for ex situ conservation of threatened or DD (Data Deficient) species whose conservation in the wild is unlikely in the near future.
Key Words: New World primates, Neotropics, ex situ population, husbandry, conservation
Resumen
Los studbooks son bases de datos de registros genealógicos individuales en poblaciones ex situ. Puesto que son una herra- mienta esencial en planeación y manejo, realizamos una búsqueda de reportes de studbooks para explorar tendencias his- tóricas en programas de cría de primates neotropicales y sus implicaciones en conservación ex situ. Accedimos a dos bases de datos: una construida por La Asociación Mundial de Zoológicos y Acuarios (WD) y otra compilada a partir de registros públicos (PD). WD comprendió 104 reportes (1998-2011) de tres regiones hábitat y siete no hábitat para 44 especies. PD consistió en 222 reportes de 34 especies de dos regiones hábitat y tres no hábitat (1973-2019). Los studbooks internacio- nales fueron más frecuentes en PD (82 %), mientras que los regionales lo fueron en WD (55.8 %). Ambas bases de datos mostraron que las categorías de la UICN (LC, NT, VU, EN, CR y DD) con un mayor número de especies contienen un mayor número de especies con studbooks y un mayor número de studbooks. Por lo tanto, existe un sesgo hacia un mayor número de studbooks in especies LC (Preocupación Menor). A pesar de las limitaciones en la disponibilidad y acceso a registros de studbooks, nuestros resultados revelaron una discrepancia entre las regiones donde se han llevado a cabo acciones de conservación in situ y de conservación ex situ. Esto resalta la necesidad de la cooperación internacional para fortalecer los esfuerzos de conservación, construir infraestructura, incrementar los tamaños efectivos poblacionales y en últimas establecer poblaciones viables. Finalmente, recomendamos evaluar oportunidades de conservación ex situ de especies amenazadas DD (Datos Deficientes) cuya conservación en el medio silvestre es improbable en el futuro cercano.
Palabras Clave: Primates del Nuevo Mundo, Neotrópico, poblaciones ex situ, cría en cautiverio, conservación
Introduction release or reintroduction (Pelletier et al., 2009; Dulloo et al., 2010; Leus, 2011). Such is the emblematic case of the Captive breeding of wild species has conferred a remarkable golden lion tamarin (Leontopithecus rosalia), whose conser- alternative for conservation of threatened species through vation program achieved a population recovery and status establishment of populations in controlled environments, change from Critically Endangered to Endangered (Soo- and it has been seen as a potential source of specimens for rae, 2010; Kierulff et al., 2012). In fact, the International Neotropical Primates 26(1), September 2020 31
Union for Conservation of Nature (IUCN) has formulated disregarded. Indeed, it has become a sensible or even an guidelines to help identify in five steps those cases when unavoidable alternative (Lascuráin et al., 2009; Pelletier et ex situ management might be an appropriate conservation al., 2009; Dulloo et al., 2010; Leus 2011; Soto-Calderón strategy (IUCN/SSC, 2014). Since the first signatories to et al., 2015). the Convention on International Trade in Endangered Spe- cies of Wild Fauna and Flora (CITES) in the 1970s, zoos An essential tool for successful establishment and man- and animal parks have managed to establish ex situ popula- agement of ex situ populations is the studbook (Conway, tions of species whose collection from the wild is no longer 1986; Glatston, 1986). It consists of a database with up- permitted (Gippoliti, 2012; Bowkett, 2014; Gilbert et al., dated individual records for age, sex, location, genealogical 2017; CITES, 2019). relationships, and survival. These records are necessary to estimate demographic and genetic parameters, make man- During the transition to CITES, research centers of Ne- agement decisions, and ultimately develop viable ex situ otropical primates mainly in the USA and Europe also populations, while minimizing the risk of inbreeding and established ex situ breeding programs for a variety of pur- erosion of genetic variation (Glatston, 1986, 2001; Valeg- poses including scientific and medical research (Gozalo and gia et al.,1999). Unfortunately, studbook databases are fre- Montoya, 1990; Johnsen et al., 2012). Ex situ colonies of quently restricted to regional communities or experts; thus, New World primates include marmosets, tamarins, squir- identification of trends in species of interest and temporal rel monkeys, owl monkeys, capuchins and titi monkeys variation in such cases are hardly traceable. (Tardif et al., 2006; Smith, 2012; European Association of Zoos and Aquaria, 2019; NPRC, 2019). These non-con- Given the importance of studbooks as an essential tool in servation-oriented centers have allowed the gathering of the establishment and management of ex situ populations, relevant information of interest to conservation, in areas re- we conducted a review of available studbook reports associ- lated to social behavior, reproductive biology, parasitology, ated with Neotropical primate breeding programs to iden- physiology and ecology, but they have also served as a tool tify historical emphasis on particular taxa, species of in- for education in conservation, and professional training terest for conservation, and level of collaboration between (Mittermeier et al., 1994; Giovanini, 2002; Weigl, 2005; institutions from different regions. We also considered the Nuss and Warneke, 2010; Brito et al., 2010). implications of such trends for future conservation of Ne- otropical primates. Nonetheless, the role of captive breeding programs of wild- life species in conservation has been criticized for: (1) the Methods potential emergence of demographic problems caused by the small size of ex situ populations, which makes them A database of Neotropical primate studbooks released prone to rapid loss of genetic diversity (genetic drift) and between 1998 and 2011 was kindly provided by Laurie overall fitness reduction (inbreeding depression) (Thornhill, Bingaman Lackey (WAZA, the World Association of Zoos 1993; Snyder, et al., 1996); (2) the aptitude of captive bred and Aquariums) as part of the WAZA Studbook Library animals for release can also be compromised by their physi- (WAZA, 2011); hereafter the WAZA or WD database. We ological, morphological and behavioral adaption to captive also compiled an alternative database from public sources environments. Several traits may include adaptation to and peer-reviewed journals (the Public database or PD), confinement, tameness and adaptive response to prevalent consisting of studbook reports starting with the first availa- parasites in such environments, an effect that increases with ble studbook record found, continuing up to 2019. To do the number of generations a species spends in captivity (De this, we used “Studbook + Genus name” or “Breeding pro- Vleeschouwer et al., 2003; O’Regan and Kitchener, 2005; gram (in English) + Genus name” as key phrases in Google, Williams and Hoffman, 2009); (3) limited knowledge of Google Scholar and Scopus databases. We also retrieved target populations where animals are released (Snyder et studbook reports from all of the editions of the Interna- al., 1996). Also, political instability and budget constraints tional Zoo Yearbook and from the list of references in sci- have been argued as factors that can hamper the manage- entific publications. A complete list of records is available ment of ex situ populations in the long term. from the authors upon request.We classified studbooks in both databases by taxon (subspecies, species or genus), year Despite some criticism of captive breeding programs of publication and country. Studbooks at the genus level as a recovery strategy and recognized issues of this prac- with no indication of the species were excluded (Ateles spp., tice, effective in situ conservation of primate species, i.e., Cebus spp., Aotus spp., and Callicebus spp.). We categorized conservation in their native habitats, may be unrealistic a studbook as regional when target populations were locat- in areas with heavy disturbance or loss of native habitat. ed in zoos or animal parks in a single country; otherwise, Around 40 % of the Neotropical primates (Platyrrhini) are we classified it as international. Since records frequently threatened, mainly due to habitat loss and fragmentation fail to distinguish between new studbooks and updates, (Mittermeier et al., 2009; Dulloo et al., 2010; Laurance we treated every record as an independent report (Supple- et al., 2014; Estrada et al., 2017), and therefore establish- mentary Fig. 1). We followed the taxonomy and Red List ment of healthy populations in captivity may no longer be categories of The International Union for Conservation of 32 Neotropical Primates 26(1), September 2020
Nature (IUCN) as of April the 8th 2020 (Supplementa- three (6.8 %) were assigned to other species whose taxon- ry Table 1). These categories are: Critically Endangered omy changed after the release of their studbooks (Cebus (CR), Endangered (EN), Vulnerable (VU), Near Threat- albifrons, Cebus olivaceus and Pithecia pithecia). No reports ened (NT), Least Concern (LC) and Data Deficient (DD), for DD species were recorded in this database (Table 1). A considering VU, EN, and CR as increasing threat levels for total of 65 studbooks (62.5 %) were compiled for threat- extinction. We used a Spearman-rank correlation (rs) to ened taxa. Also, 34 reports (32.7 %) corresponded to LC test the hypothesis that IUCN levels with larger number of taxa and one (1.0 %) to NT (Table 1). We observed a sig- species also contain larger numbers of assessed species and nificant correlation between the total number of species in studbook reports. We evaluated differencesin the number each IUCN threat level with both the number of managed of reports and managed taxa for each threat level between species (rs = 0.94, p = 0.017) and the number of studbook the two databases with Fisher’s Exact tests. The authors reports (rs = 0.89, p = 0.033). declare that they have no conflict of interest. Table 1. Number of Neotropical primate taxa in the IUCN Red Results List of Species with their corresponding number of studbook reports, available in the WAZA (WD) and in the Public (PD) WAZA Database (WD) databases. We identified 104 studbook reports for 44 Neotropical primate species in the 14-year period spanned by this da- WD PD tabase (1998-2011) (Supplementary Fig. 2A). This list in- No. Taxa No. Reports No. Taxa No. Reports cludes single reports for Cebus olivaceus in 2007 and Cebus (%) (%) (%) (%) albifrons in 2010, and two reports for Pithecia pithecia in LC 16 (36.4) 34 (32.7) 14 (41.2) 71 (32.0) 2009 and 2011; each of these taxa were split into sever- al species after the release of such studbooks (Boubli et NT 1 (2.3) 1 (1.0) 1 (2.9) 3 (1.4) al., 2012; Marsh, 2014; Lima et al., 2017). Institutions VU 10 (22.7) 21 (20.2) 6 (17.6) 34 (15.3) from different locations in three habitat countries (Brazil, EN 9 (20.5) 28 (26.9) 7 (20.6) 65 (29.3) Colombia and Costa Rica) and seven non-habitat regions CR 5 (11.4) 16 (15.4) 5 (14.7) 38 (17.1) (USA, Europe, New Zealand, Mexico, Colombia, Australia Other * 3 (6.8) 4 (3.8) 1 (2.9) 11 (5.0) and Japan) compiled these reports through regional efforts or international collaboration in 58 (55.8 %) and 46 cases Total 44 104 34 222 (44.2 %), respectively. The most productive regions were LC: Least Concern; NT: Near Threatened; VU: Vulnera- Europe and the USA, with a total of 79 records (76 %) ble; EN: Endangered; CR: Critically Endangered. * Species for 42 of the 44 Neotropical primate taxa in the database. reclassified as two or more species since studbook report. These regions were followed by institutions from Japan and Brazil, each with six studbook reports for a total of 12 dif- Of the 104 reports in WD, we had to exclude 23 records ferent primates (Supplementary Fig. 2A). with unavailable publication date from yearly statistics. Of the remaining 81, the average annual number of reports Reports from habitat countries included the black lion was 5.8 (S.D. = 5.9), with the highest number of reports in tamarin (Leontopithecus chrysopygus), the crested capuchin 2006 and 2010 with 18 reports for each year, followed by (Sapajus robustus), the Peruvian spider monkey (Ateles cha- 2009 with ten and 2011 with eight (Supplementary Fig. mek), the white-fronted spider monkey (A. belzebuth), the 1A). We found no records for the 1999-2000 period. The black spider monkey (A. paniscus) and the white-cheeked first set of reports for Neotropical primates was published spider monkey (A. marginatus) in Brazil; the cotton-top in 1998 for spider monkeys (Ateles chamek, A. geoffroyi, A. tamarin (Saguinus œdipus), the white-footed tamarin (S. belzebuth and A. fusciceps). The most recentreports were leucopus) and the black-handed spider monkey (A. geof- published in 2011 for the pygmy marmoset (Cebuella froyi) in Colombia; and the Central American squirrel pygmaea), the cotton-top tamarin (Saguinus œdipus), the monkey (Saimiri œrstedii) in Costa Rica. Several taxa stand black-headed night monkey (Aotus nigriceps), the south- out with five studbook reports, as in the case of Saguinus ern night monkey (A. azarae), the grey-legged douroucou- œdipus with three regional (Australia, Colombia and Ja- li (A. lemurinus), the white-faced saki (Pithecia pithecia), pan) and two international studbook reports, as well as A. the white-headed marmoset (Callithrix geoffroyi), and the geoffroyi with three regional (New Zealand, USA and Co- black-handed spider monkey (Ateles geoffroyi). lombia) and two international reports from Europe. The genus with the most reports is Ateles with 30, followed by Public Databases (PD) Saguinus with 17. We found a total of 222 studbook reports produced be- tween 1973 and 2015 for 34 species, including eight stud- Of the 44 Neotropical primate species with at least one book reports for Pithecia pithecia that were released before studbook report, 24 species (54.5 %) were classified under this species was divided into two species P. pithecia and P. an increased threat level (VU, EN, or CR), 16 (36.4 %) were chrysocephala more recently (Marsh, 2014). These stud- categorized as LC, one (2.3 %) as NT and the remaining books were compiled by institutions in three non-habitat Neotropical Primates 26(1), September 2020 33
(USA, Europe and Australia) and two habitat regions (Bra- albifrons, Cebus olivaceus and Pithecia pithecia) had at least zil and Colombia) (Supplementary Fig. 2B). Institutions one studbook in either of the two databases. LC contains from non-habitat regions, mainly Europe and the USA, the largest number of species with at least one studbook have participated in the development of 94.6 % (210) of all (17, 37.8 %). A total of 27 threatened species (VU, EN reports at both regional and international levels. We iden- and CR) have studbooks and represent 60.0 % of all man- tified 182 (82.0 %) international reports for 32 taxa, and aged species. We failed to find active studbooks for three 40 (18.0 %) regional reports from habitat and non-habitat threatened species that had been previously managed (Sup- countries for 16 taxa (Supplementary Fig. 2B). Only elev- plementary Figure 1B). The most concerning case is the en studbook reports were developed in habitat countries, Wied’s marmoset (Callithrix kuhlii), which seems to have including seven for the black lion tamarin (Leontopithecus a single regional studbook issued in 2003. The two other chrysopygus) endemic to Brazil, along with three for the threatened species are the Geoffroy’s spider monkey (Ateles white-footed tamarin (Saguinus leucopus) and one for the geoffroyi) and the common woolly monkey (Lagothrix lago- brown-headed spider monkey (Ateles fusciceps) endemic to thricha), with studbooks issued in 2010 and 2017, respec- Colombia. Two tamarins (L. rosalia and S. œdipus) and one tively. Only five out of 18 CR species have been managed howler monkey (Alouatta caraya) stand out for having the (27.8 %), all with actively updated studbooks in European largest number of studbook reports, mostly developed in zoos (Fig. 1 and Supplementary Table 1). The 13 CR spe- non-habitat countries. The genus with the most studbook cies with no record of previous management were the fol- reports was Leontopithecus with 40, followed by Saguinus lowing: the black-faced lion tamarin (Leontopithecus cais- with 32. sara), the Ecuadorian capuchin (Cebus aequatorialis), the ka’apor capuchin (C. kaapori), the Trinidad white-fronted Among the 34 taxa with at least one studbook report in capuchin (C. trinitatis), the blond capuchin (Sapajus flavi- PD, the Red List category with the largest representation us), Barbara brown’s titi (Callicebus barbarabrownae), the was LC with 14 taxa (41.2 %), followed by 18 species clas- Caqueta titi (Plecturocebus caquetensis), the Rio Mayo titi sified under an increased threat level (52.9 %), one NT (P. oenanthe), the black-bearded saki (Chiropotes satanas), (2.9 %), and one remaining species with recent taxonom- the northern muriqui (Brachyteles hypoxanthus), the south- ical changes (2.9 %) (Table 1). No DD taxa were present ern muriqui (B. arachnoides), the Colombian woolly mon- in this database. Threatened taxa were represented by 137 key (Lagothrix lugens) and the yellow-tailed woolly monkey reports (61.7 %), LC by 71 reports (32.0 %), NT by three (L. flavicauda). (1.4 %) and other taxa by 11 reports (5.0 %) (Table 1). The number of studbooks but also the number of managed spe- cies in each IUCN level increased with the total number of species in each level, but this relationship was only signifi- cant in the second case (rs = 0.89, p = 0.033).
The average number of reports per year was 4.63 (S.D. = 6.07) starting in 1973 with a studbook compiled for the golden lion tamarin (Leontopithecus rosalia) (Jones, 1973). The most recent reports were released in 2019 for 28 species (Supplementary Fig. 1B). The most productive years were 2016, 2017 and 2019. We found no publica- tions for 1974 and 1975. Only one studbook report in PD was missing the date of release. Figure 1. Number of Neotropical primates with presence versus absence of at least one previous studbook (ST), for each IUCN Combined databases category. The left Y-axis indicates the number of species, and the We detected no differences between the two databases, right Y-axis the proportion of species with at least one studbook neither in the number of reports for species in each Red for each IUCN category. LC: Least Concern; NT: Nearly Threat- List category (Fisher´s test, p = 0.704) nor in the number of ened; VU: Vulnerable; EN: Endangered; CR: Critically Endan- gered; DD: Data Deficient. managed species in such categories (Fisher’s test, p = 0.992). However, a comparison of the two databases for the same time frame (1998-2011) showed that WD was more geo- Discussion graphically diverse and covered more taxa than public da- tabases. WD comprised reports from New Zealand, Japan, We searched for studbook reports of Neotropical primate Mexico, and Costa Rica that were unavailable in PD. Also, species as a means to identify husbandry programs and di- WD comprised a larger number of species for this time agnose their current and/or future use in conservation. We period, including all the taxa present in PD. are aware that our results do not reflect the actual number of studbooks but instead, the number of reports of ex situ A total of 45 (27.8 %) out of 162 Neotropical primate breeding programs of Neotropical primate species based on species recognized in the Red List (after excluding Cebus two independent sources of information. Since studbooks 34 Neotropical Primates 26(1), September 2020 are not an obligation but a service that institutions provide Colombia and Peru (Güneralp and Seto, 2013; Estrada et free of charge to peer institutions (Glatston, 1986), stud- al., 2017). Once again, cooperation between institutions book updates are not necessarily reported or accessible and from habitat and non-habitat countries could be quite ad- they may not contain comprehensive information regard- vantageous, in this case to integrate in situ conservation ing studbook keepers or host institutions. This limitation efforts inthe Neotropics with scientific research and infra- prevented us from distinguishing between novel studbooks structure derived from ex situ populations (European Asso- and updates of previous studbooks, and there was no un- ciation of Zoos and Aquaria, 2019). equivocal way to validate simultaneous reports of a given studbook in the two databases; i.e. those present in both The fact that threatened New World primate species ac- PD and WD databases. However, we were able to identify count for 60 % of all species with previous studbooks similar trends in both databases, but also compare temporal shows that management of ex situ populations may have a variations in the number of reports and emphasis made on remarkable impact on conservation of threatened species. particular taxa. However, a previous survey of birds and mammals showed that species in zoos are less threatened than related species Both databases comprised studbook reports exclusively not held in zoos (Martin et al., 2014). Among the 18 CR produced by zoos around the world, since studbooks devel- Neotropical primate species, only five have been the target oped by non-zoo institutions were unavailable and there- of a studbook because in addition to conservation purpos- fore out of the scope of this review. This is unfortunate es, other reasons and motivations may guide the decision because, despite the relevance of scientific knowledge from to whether or not to establish a studbook of a given species research centers in understanding the biological require- (Mendes et al., 2008; Estrada et al., 2017; IUCN, 2017). ments of species for reproduction in captivity and their Some of these include the cost to keep an ex situ popula- potential for in situ conservation, integration with efforts tion in captivity, preference for more charismatic species from zoos and other conservation-oriented institutions to attract visitors or restrictions to access species of interest seems to be only occasional, if not entirely missing. (Bowkett, 2014; Fa et al., 2014). In fact, the two databases compiled in this study revealed that the larger the number Most studbook reports in PD are international, whereas of species in a given IUCN level, the larger the number those in WD were mainly regional. The fact that interna- of species with at least one studbook and the larger the tional studbooks require stronger collaboration of stake- number of studbooks. This explains the overrepresentation holders, and as a consequence, they have more visibility in of studbooks and managed species in LC as compared to international journals and other sources available on inter- other levels, a pattern also seen in other vertebrates (Ober- net, may account for the high percentage of international wemmer et al., 2011). studbooks in PD. This contrasts with the higher prevalence of regional studbooks in WD. A similar pattern was found Changes in IUCN categorization and taxonomy also may in other monitored taxa in WAZA zoos, where only 15 % explain the deficit of studbooks in certain species, and ar- of studbooks are international (Traylor-Holzer, 2011), in- guably of ex situ populations. The genusCebus is a taxon dicating that management efforts are mainly conducted at with intricate phylogeography whose taxonomy and sys- the regional level. Information for specific animal species tematics has undergone radical changes over the past few in zoos around the world is available to the WAZA com- years (Boubli et al., 2012; Lima et al., 2017). In particular, munity through international studbook reports (WAZA, a studbook for the capuchin monkey Cebus olivaceus was 2018). This may be used to foster integration of efforts released in 2007, but this taxon is in process of being di- from local, regional and international stakeholders to in- vided into multiple species including C. olivaceus, C. brun- crease effective population sizes through careful metapop- neus, C. castaneus, and the critically endangered C. kaapori, ulation management, and in so doing improve the genetic all of which lack a subsequent studbook. Likewise, the and demographic health of established populations and capuchin monkeys Cebus albifrons, C. versicolor, C. aequa- their expected viability to the long term. torialis, C. cesarae, C. trinitatis, C. cuscinus and C. mali- tiosus were all subsumed within C. albifrons until recently; Our results showed that institutions from countries in the a taxonomic change that took place after the release of a Neotropics have led only a minority of studbooks, which studbook for this species in 2010. Similarly, Pithecia pithe- uncovers a disparity between regions where captive breed- cia was recently split in P. pithecia and P. chrysocephala, after ing has been stressed and those where in situ conservation the release of multiple studbooks between 1989 and 2011 efforts are required. This is strongly influenced by differ- (Marsh, 2014). Following these taxonomic changes, it ences in financial resources and infrastructure between turned out that several newly named species were classified regions, since primate habitats are mostly located in de- as threatened, and it is probably too early to have managed veloping countries with less financial capacity, staff and the foundation of new ex situ populations (e. g., C. aequa- infrastructure (Cuarón, 2005). Also, recent simulations torialis, C. malitiosus, C. versicolor, C. trinitatis, C. kaapori, forecast a growing conflict caused by agricultural and hu- and Pithecia chrysocephala). Similar cases are the critical- man expansion in areas of high primate species richness ly endangered blond capuchin Sapajus flavius, which was in the Neotropics, especially in countries such as Brazil, recently rediscovered (Oliveira and Langguth, 2006), the Neotropical Primates 26(1), September 2020 35 two species of muriqui (Brachyteles arachnoides and B. hy- Boubli, J. P., Rylands, A. B., Farias, I. P., Alfaro, M. E., and poxanthus), formerly considered the same species (Groves, Alfaro, J. L. 2012. Cebus Phylogenetic Relationships: A 2001; 2005), and lastly the titi monkeys with at least nine Preliminary Reassessment of the Diversity of the Untuft- new species of Callicebus and Plecturocebus described since ed Capuchin Monkeys. Am. J .Primatol. 74(4): 381–393. 2010 (Wallace et al., 2006; Defler et al., 2010; Byrne et al., Bowkett, A. 2014. Ex situ conservation planning is more 2016; Boubli et al., 2019; Mittermeier and Rylands, 2020). complicated than prioritizing the keeping of threatened species in zoos. Anim. Cons. 17(2): 101–103. We found no studbooks of DD species in our data. Many Brito, D., Ambal, R. G., Brooks, T., Silva, N. De, Foster, of these are highly endemic or distributed in relatively re- M., Hao, W., … and Rodríguez, J. V. 2010. How similar mote areas, with limited or untested survival and/or repro- are national red lists and the IUCN Red List? Biol. Con- ductive success in captivity (Müller et al., 2011; Martin et serv. 143(5): 1154–1158. al., 2014a). As a consequence, specimens and ex situ pop- Byrne, H., Rylands, A. B., Carneiro, J. C., Alfaro, J. W. ulations of these primates are also virtually absent in zoos. L., Bertuol, F., da Silva, M. N. F., … and Boubli, J. P. Within DD taxa are for instance several species of Pithecia 2016. Phylogenetic relationships of the New World titi and Plecturocebus that have been recently described or Ao- monkeys (Callicebus): First appraisal of taxonomy based tus, such as A. zonalis and A. jorgehernandezi that have been on molecular evidence. Front. Zool. 13(1): 1–26. poorly studied in the field (Defler, 2010; Marsh, 2014; CITES. 2019. Resolutions of the Conference of the Parties Byrne et al., 2016). in effect after the 17th meeting | CITES. Accessed July 22, 2019, https://www.cites.org/eng/res/index.php Since habitat loss poses the main threat for conservation Conway, W. G. 1986. The practical difficulties and finan- of Neotropical primates, it is important to scrutinize the cial implications of endangered species breeding pro- pertinence and viability of prioritizing ex situ conserva- grammes. Inter. Zoo Yearb. 24(1): 210–219. tion programs for the most threatened taxa (Estrada et al., Cuarón, A. D. 2005. Further role of zoos in conservation: 2017). Along with protection of native habitats, ex situ Monitoring wildlife use and the dilemma of receiving do- conservation may be a plausible conservation alternative for nated and confiscated animals.Zoo Biol. 24(2): 115–124. species such as the black-faced lion tamarin (Leontopithecus De Vleeschouwer, K., Leus, K., and Van Elsacker, L. 2003. caissara), the blond titi (Callicebus barbarabrownae), the Characteristics of reproductive biology and proximate Caquetá titi (Plecturocebus caquetensis) and other CR spe- factors regulating seasonal breeding in captive gold- cies with no studbooks or managed populations, whose es- en-headed lion tamarins (Leontopithecus chrysomelas). timated population sizes have fallen to critically low num- Am. J Primatol. 60(4): 123–137. bers with a steady trend to decline (Lorini and Persson, Defler, T. R. 2010. Historia natural de los primates colom- 1994; García et al., 2010; Printes et al., 2011). Should bianos. Universidad Nacional de Colombia. Bogotá DC, conservation strategies of these species rely on ex situ pop- Colombia. ulations in the near future, they will depend on careful pri- Defler, T. R., Bueno, M. L., and García, J. 2010. Callicebus oritization of target species for conservation, identification caquetensis: A New and Critically Endangered Titi Mon- of in situ and ex situ strategies, the availability of resources key from Southern Caquetá, Colombia. Primate Conserv. to invest in building infrastructure and research in repro- 25(1): 1–9. ductive biology and creation of collaborative international Dulloo, M. E., Hunter, D., and Borelli, T. 2010. Ex Situ networks (Martin et al., 2014b). and In Situ Conservation of Agricultural Biodiversity: Major Advances and Research Needs. Not. Bot. Horti Acknowledgements Agrobot. Cluj-Napoca 38(2): 123–135. Estrada, A., Garber, P. A., Rylands, A. B., Roos, C., Fer- We are grateful to Laurie Bingaman Lackey for granting nandez-Duque, E., Di Fiore, A., … and Li, B. 2017. 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Supplementary Table 1. List of Neotropical primate taxa with at least one studbook record, sorted by IUCN conservation status.
IUCN Status Taxa with no studbook Taxa with studbook IUCN Status Taxa with no studbook Taxa with studbook
Brachyteles arachnoides Ateles fusciceps Alouatta arctoidea Alouatta caraya Brachyteles hypoxanthus Ateles hybridus Alouatta guariba Aotus azarae Callicebus Saguinus bicolor Alouatta juara Aotus nigriceps barbarabrownae Cebus aequatorialis Saguinus œdipus Alouatta macconnelli Aotus vociferans Cebus kaapori Sapajus xanthosternos Alouatta nigerrima Callithrix geoffroyi Cebus trinitatis Alouatta palliata Callithrix jacchus CR Chiropotes satanas Alouatta puruensis Callithrix penicillata Lagothrix flavicauda Alouatta sara Cebus capucinus Lagothrix lugens Alouatta seniculus Mico argentatus Leontopithecus caissara Aotus trivirgatus Plecturocebus cupreus Plecturocebus caquetensis Cacajao melanocephalus Plecturocebus LC donacophilus Plecturocebus oenanthe Callibella humilis Saguinus imperator Sapajus flavius Cebus brunneus Saguinus labiatus Alouatta pigra Ateles belzebuth Cebus castaneus Saguinus midas Alouatta ululata Ateles chamek Cheracebus lucifer Saimiri boliviensis Aotus miconax Ateles geoffroyi Cheracebus lugens Saimiri sciureus Callicebus coimbrai Ateles marginatus Cheracebus purinus Sapajus apella
EN Cebus malitiosus Callithrix aurita Cheracebus regulus Cebus versicolor Callithrix flaviceps Cheracebus torquatus Chiropotes albinasus Leontopithecus Chiropotes chiropotes chrysomelas Chiropotes utahickae Leontopithecus Leontocebus cruzlimai chrysopygus 38 Neotropical Primates 26(1), September 2020
IUCN Status Taxa with no studbook Taxa with studbook IUCN Status Taxa with no studbook Taxa with studbook
Lagothrix cana Leontopithecus rosalia Leontocebus fuscus EN Plecturocebus modestus Saguinus leucopus Leontocebus illigeri Plecturocebus olallae Sapajus robustus Leontocebus lagonotus Alouatta belzebul Aotus griseimembra Leontocebus leucogenys Alouatta discolor Aotus lemurinus Leontocebus nigricollis Aotus brumbacki Aotus nancymaae Mico acariensis Cacajao ayresi Ateles paniscus Mico chrysoleucos Callicebus melanochir Cacajao calvus Mico emiliae Callicebus personatus Cacajao hosomi Mico intermedius Cebus leucocephalus Callimico goeldii Mico mauesi VU Cheracebus medemi Callithrix kuhlii Mico melanurus Lagothrix poeppigii Cebuella pygmaea Mico saterei Mico leucippe Lagothrix lagothricha Pithecia aequatorialis Mico rondoni Saimiri œrsteddi Pithecia albicans Pithecia mittermeieri Pithecia chrysocephala Plecturocebus ornatus Pithecia inusta Saguinus niger Pithecia monachus Saimiri vanzolinii Pithecia napensis Callicebus nigrifrons Saguinus geoffroyi Plecturocebus LC aureipalatii Cebus cuscinus Plecturocebus baptista Leontocebus tripartitus Plecturocebus bernhardi Mico nigriceps Plecturocebus brunneus NT Saguinus martinsi Plecturocebus caligatus Saimiri ustus Plecturocebus cinerascens Sapajus libidinosus Plecturocebus discolor Sapajus nigritus Plecturocebus dubius Aotus jorgehernandezi Plecturocebus hoffmannsi Aotus zonalis Plecturocebus moloch Cebus cesarae Plecturocebus pallescens Mico humeralifer Saguinus fuscicollis Mico marcai Saguinus inustus Pithecia cazuzai Saguinus melanoleucus Pithecia hirsuta Saguinus mystax DD Pithecia irrorata Sapajus cay Pithecia isabela Sapajus macrocephalus Pithecia milleri Pithecia pissinattii Pithecia vanzolinii Cebus albifrons Plecturocebus stephennashi Other * Cebus olivaceus Plecturocebus vieirai Pithecia pithecia
IUCN status (2020): CR (Critically Endangered), EN (Endangered), VU (Vulnerable), NT (Nearly Threatened), DD (Data Deficient) and LC (Least Concern). * Species reclassified as two or more species since studbook report. Neotropical Primates 26(1), September 2020 39
Supplementary Figure 1. Temporal trend in studbook reports of Neotropical primate taxa.
A. Reports in the WAZA (WD) database released between 1998 and 2011. * Species reclassified as two or more species since stud- book report.
B. Reports in the Public database (PD) released between 1973 and 2019. Regional (light gray) and international (dark gray) stud- books are categorized according to the species and the year in which they were published. Colored cells indicate single records unless indicated otherwise. * Studbooks released before split into several species. 40 Neotropical Primates 26(1), September 2020
Supplementary Figure 2. Representation of 48 Neotropical primate taxa in studbook reports published across different countries and regions. A. Records between 1998 and 2011 in the WAZA database (WD). * Studbooks are categorized by family, taxon and location of the chief orga- nization involved in the development of each studbook.
B. Records between 1973 and 2019 in the Public database (PD). * Studbooks released before introduc- tion of taxonomic changes. Neotropical Primates 26(1), September 2020 41
OCORRÊNCIA, ECOLOGIA E CONSERVAÇÃO DO GUIGÓ-DA-CAATINGA (CALLICEBUS BARBARABROWNAE - HERSHKOVITZ, 1990)
Udemario Maia Ribeiro1, José Monteiro do Nascimento Junior2, Francisco Mário Fagundes Barbosa3 e Marcos Roberto Rossi dos Santos4
1 Mestrado Profissional em Ecologia Aplicada à Gestão Ambiental - Universidade Federal da Bahia, Laboratório de Ecologia Acústica e Comportamento Animal – Universidade Federal do Recôncavo da Bahia, e-mail:
Resumo
O guigó-da-caatinga, Callicebus barbarabrownae - Hershkovitz 1990, é o único primata endêmico do bioma caatinga no nordeste da Bahia. A espécie encontra-se ameaçada de extinção pela perda de habitat, causada principalmente pela supres- são da vegetação e fragmentação das florestas onde se encontram. O presente estudo teve como objetivo localizar, com o auxílio de playback, e registrar os fragmentos ocupados por grupos de guigós no município de Banzaê, Bahia – Brasil. Além do registro de novas áreas de ocorrência, foi descrita a utilização de frutos dos gêneros Capparis (Brassicaceae) e Manilkara (Sapotaceae) pelos guigós.
Palavras-chave: Primatas, extinção, Banzaê
Abstract
The blonde titi-monkey,Callicebus barbarabrownae - Hershkovitz 1990, is the only primate endemic to the Caatinga biome in northeastern Bahia. The species is threatened with extinction due to habitat loss, mainly caused by vegetation suppres- sion and fragmentation of the forests in which they are found. The aim of the present study was to locate, with the aid of playback, and to record the fragments occupied by groups of titis in the city of Banzaê, Bahia, Brazil. In addition to documenting new occurrence localities, the use of fruits of the genera Capparis (Brassicaceae) and Manilkara (Sapotaceae) was described.
Key Words: Primates, extinction, Banzaê
Introdução Geoffroy, 1812). Poucos estudos relacionados à espécie po- dem ser encontrados, o que a torna uma espécie ainda mais A Caatinga no nordeste brasileiro ainda é um bioma pouco fragilizada e ameaçada de extinção. O desconhecimento estudado. No entanto, apesar da escassez de conhecimentos sobre essa espécie inviabiliza ações que possam contribuir sobre sua biodiversidade, a Caatinga se apresenta ameaçada para a sua preservação. Um dos principais fatores responsá- e fragmentada, contrastando com a sua relevância biológica veis pela redução populacional em primatas não humanos o bioma pode ser considerado um dos mais ameaçados do é o desmatamento e a consequente perda de habitat (Isa- Brasil (Leal et al., 2003). Poucos são os mamíferos endê- birye-Basuta e Lwanga, 2008; Kierulff et al., 2012; Hilário micos da Caatinga (Leal et al., 2003). Dentre essas espécies et al., 2017). Muitas das espécies do gênero Callicebus es- está o guigó da caatinga (Callicebus barbarabrownae – Her- tão ameaçadas de extinção, devido à destruição do habitat, shkovitz, 1990) (Veiga et al., 2008; Gutiérrez e Marinho- desmatamento e caça (Nagy-Reis, 2012). -Filho, 2017), habitando fragmentos de caatinga no estado da Bahia, é ainda o símbolo de resistência à insensatez e à Na mais recente revisão (Byrne et al., 2016) o gênero Calli- destruição humana. cebus, que anteriormente abrangia 34 espécies distribuídas geograficamente desde a região sudeste do Brasil à floresta Considerada como espécie a partir de 2002 (Printes, 2007), amazônica, ficou restrito às espécies da faixa litorânea bra- Callicebus barbarabrownae foi descrita por Philip Hershko- sileira entre os estados de Sergipe e São Paulo. Permane- vitz (1990) como uma subespécie de C. personatus (E. cem distribuídos no gênero Callicebus apenas as espécies do 42 Neotropical Primates 26(1), September 2020 grupo personatus: C. melanochir, C. personatus, C. nigrifrons, C. coimbrai e C. barbarabrownae. Com exceção de C. bar- barabrownae, as outras espécies do gênero ocupam porções da Mata Atlântica (Culot et al., 2019). C. barbarabrownae está restrito à caatinga da região nordeste do Brasil entre os estados de Bahia e Sergipe.
Callicebus configura-se como um gênero predominante- mente arborícola, ocupando os extratos de médio ao baixo das florestas, dificilmente descendo ao solo. Alimenta-se preferencialmente de frutos, folhas ou flores, e nos períodos de escassez destes itens pode incluir insetos em sua dieta (Souza Alves, 2010, 2011). Figura 1. Mapa de localização do município de Banzaê, elaborado O objetivo desse trabalho foi localizar e registrar a ocor- a partir de banco de dados do Instituto Brasileiro de Geografia rência dos guigós, em fragmentos de Caatinga. Mapear e Estatística – IBGE, e Fundação Nacional do Índio – FUNAI. a distribuição desses grupos de guigós é fundamental para a tomada de decisões na escolha de grupos mais propícios O município de Banzaê (Fig. 1) está inserido no “Polígono para prosseguir com pesquisas relacionadas à conservação das Secas”, apresentando um clima do tipo megatérmico dos habitats e à ecologia da espécie. semiárido, com temperatura média anual de 24.3°C, pre- cipitação pluviométrica média no ano de 600 a 800 mm e Materiais e métodos período chuvoso de maio a julho (CPRM, 2005). A popu- lação estimada é de 13,229 pessoas, e a área do município Área de estudo é de 409,507 km² (IBGE, 2019). De acordo com o Censo A escolha do município se deu através de um encontro de Agropecuário de 2006, o município possuía um rebanho Educação Ambiental, promovido pelo Governo do Estado bovino de 12.895 cabeças, caprinos 1,231, equinos 682 e da Bahia, através Fundação Luís Eduardo Magalhães e a Se- ovinos 4.289 (IBGE, 2006). cretaria de Meio Ambiente do estado. Realizado na cidade de Tucano, no mesmo estado, estavam presentes represen- Procedimentos de campo tantes de órgãos públicos e sociedade civil, envolvidos em Foram feitos contatos com alguns moradores da região - ações ambientais. Participaram desse encontro entre 15 e preferencialmente moradores da zona rural que nasceram, 20 pessoas oriundas de municípios da região do semiárido e/ou, tenham residido a maior parte de sua vida na região baiano (Banzaê, Tucano, Serrinha, Coronel João Sá, Cícero - através de contato direto por um dos pesquisadores que Dantas, Ribeira do Pombal, Euclides da Cunha). nasceu no município e já possuía o conhecimento prévio dessas pessoas (apicultores, criadores de gado e agriculto- Durante este encontro um dos pesquisadores fez uma apre- res). Na oportunidade, foi esclarecido às pessoas com quem sentação sobre o guigó da Caatinga para os representantes mantivemos contato direto durante as pesquisas (morado- municipais e ao final foi mostrado uma imagem e aciona- res das localidades de ocorrência dos primatas e apicultores) do um playback com a vocalização do guigó. Após esse sobre a existência de uma espécie ameaçada de extinção na momento foi perguntado aos presentes sobre a existência região. Destacamos a essas pessoas o papel que a especie ou relato de existência desse primata em seus municípios. desempenha na manutenção dos ecossistemas onde habi- As respostas positivas vieram apenas dos representantes dos tam, visando com esses esclarecimentos, contribuir para a municípios de Serrinha e Ribeira do Pombal (município boa relação entre população humana e a biodiversidade. este que faz divisa com Banzaê). Pela solidez nas afirmações Populações rurais, no geral, percebem no ambiente apenas quanto aos relatos de ocorrência, optamos pelas incursões os bens naturais que podem gerar lucros ou outros benefí- no município de Banzaê. Além desta cidade já ter sido cita- cios imediatos (Torres Junior, 2015). No contato com esses da como área de ocorrência por outro pesquisador (Printes, moradores, além de apresentar imagens durante as coletas 2007, 2011). de informações, era apresentada também a vocalização da espécie. O local escolhido foi o que se mostrou mais propício à con- firmação de localização dos guigós, devido ao maior nú- Entre os meses de abril e setembro de 2016, os esforços mero de relatos de sua existência no local. Apesar desses de amostragem somaram um total de 09 dias de campo, relatos, nenhum dos informantes afirmou ter avistado a es- especificamente nas localidades com probabilidades de se pécie. A existência era confirmada apenas pela vocalização encontrar os guigós. Dias de campo, para o registro das do guigó da Caatinga. localizações e visualizações, foram feitos uma ou duas vezes por mês, com saída de Salvador com destino à Banzaê às sextas, e retorno às segundas-feiras. Neotropical Primates 26(1), September 2020 43
Como os guigós geralmente vocalizam pela manhã ou ao selva - entre as espécies. O registro da localização foi feito entardecer (Freitas, 2010; Rocha, 2011), nos dirigíamos com o GPS Garmin modelo Etrex 30. Os pontos foram ao fragmento previamente selecionado logo após o clarear marcados no aparelho e anotados em caderno de anotações do dia, entre 4:00 e 5:00 horas da manhã. O fragmento no momento da chegada ao fragmento e antes de acionar Soturno foi uma exceção, onde acampamos e dormimos o playback. no local. Utilizamos playbacks para localizar os guigos (Je- rusalinsky et al., 2006; Printes, 2011; Cäsar et al., 2012). Resultados Para o playback utilizamos vocalizações (não publicadas) de três espécies de guigós: C. coimbrai, C. nigrifrons e C. Entre o período dos levantamentos de campo os pesquisa- barbarabrownae. O áudio de C. coimbrai foi obtido no dores participaram de uma reunião na Associação de Api- município de Simões Filho, estado da Bahia, C. nigrifrons cultores de Banzaê onde puderam conversar com os apicul- proveniente do estado de Minas Gerais e C. barabara- tores locais e fazer uma breve apresentação da espécie, seu brownae no município de Lamarão estado da Bahia. Op- estado de conservação e a necessidade de preservação da tamos por acionar o playback com intervalos de cinco mi- Caatinga para a manutenção das populações de guigós na nutos entre reproduções até que a primeira resposta fosse região. Através de conversas informais, colhemos ainda al- ouvida. Após confirmação desta primeira resposta, seguí- gumas informações sobre a localização dos primatas, mas a mos o mesmo padrão de intervalos entre reproduções se maioria das pessoas desconheciam a espécie, a não ser pelos as respostas continuavam até a aproximação dos guigós. A relatos de localização e visualização por parte de um apicul- quantidade de reproduções realizadas variou em número tor indígena habitante da Reserva Kiriri. de acordo com a distância entre os pesquisadores e os gui- gós e o tempo decorrido até uma possível visualização da No total foram comprovadas 05 localidades (Tabela 1 e espécie. Após a visualização, dificilmente prosseguíamos Fig. 2) com ocorrência dos guigós no município de Ban- com o playback, a não ser que precisássemos visualizá-los zaê, sem adentrar nas terras indígenas. A localidade “So- por um período de tempo maior (para fotografar). Se as turno” já havia sido visitada anteriormente por Printes reproduções não obtinham resposta optamos também por (2007); as outras quatro são novos registros. São as se- não ultrapassar um total de dez reproduções. A resposta guintes localizações: Soturno, Retiro, Doroteia, Camamu ao playback na maioria das vezes sempre ocorria no máxi- e Grota (denominação do local dada pelos pesquisado- mo após a terceira reprodução do playback. res) próxima à zona urbana de Banzaê (em torno de 500 metros). Printes (2007) em estudos com C. barbarabrownae, utilizou a vocalização de C. personatus obtendo um bom resultado Nas Fazendas Soturno e Camamu, foram confirmadas a de respostas ao playback. No entanto, pelo fato de termos presença dos guigós em dois fragmentos separados. Na usado ao menos duas vocalizações diferentes no playback, primeira localidade, foram duas idas a campo. Na primei- não podemos tirar uma conclusão definitiva sobre o padrão ra incursão apenas ouvimos as vocalizações em resposta ao de respostas às reproduções, pois alguns fatores podem in- playback, mas na segunda ida, quando acampamos local, foi fluenciar na resposta, além da reprodução da vocalização possível a visualização de três indivíduos (Fig. 3) Na Fazen- de uma ou outra espécie. Esses fatores incluem a distância da Camamu, no primeiro fragmento visitado, obtivemos entre os pesquisadores e os grupos de guigós, a qualidade apenas resposta acústica, mas ao acionarmos o playback da reprodução, o clima ou até o contexto em que a espécie em outro fragmento um grupo vocalizou em resposta e se está inserida, tais como: local com presença humana próxi- aproximaram dos pesquisadores, permitindo assim a visu- ma e a relação destes com a espécie, a convivência pacífica alização de cinco indivíduos. Mas ao perceberem a nossa ou conturbada - caça, movimentação e fluxo de pessoas, presença, o bando se afastou em fuga. barulho excessivo ou fora dos padrões de um ambiente de
Tabela 1. Localidades e registros de vocalização e visualização de Callicebus barbarabrownae no município de Banzaê, estado da Bahia, Brasil.
Localidade Coordenadas Geográficas Vocalização Visualização Indivíduos Lat./Long. (WGS84)) visualizados
Soturno −10.59066 / −38.58969 Sim Sim 03 Retiro −10.51546 / −38.64423 Sim Sim 01 Doroteia −10.54476 / −38.65069 Sim Não 00 Camamu −10.59623 / −38.57611 Sim Sim 05 Grota prox. Zona Urbana −10.59298 / −38.60181 Sim Sim 01 44 Neotropical Primates 26(1), September 2020
Na localidade mais próxima à zona urbana de Banzaê, a qual denominamos Grota, avistamos apenas um indivíduo de Callicebus barbarabrownae. Devido às pequenas dimen- sões e ao grau de antropização do fragmento, apesar da dificuldade de penetração na mata, a manutenção de um grupo viável nesse local é quase impraticável.
Durante os meses de abril e maio encontramos vários fru- tos de icó - Capparis yco – Brassicaceae (Souza, 2008) - no fragmento Soturno, com marcas de mordidas. Esta espécie é encontrada com facilidade em todos os fragmentos visi- tados e alguns grupos de guigós foram avistados próximos ao local de frutos encontrados com mordidas recentes. No fragmento Retiro, no local de avistagem do guigó, frutos da maçaranduba - Manilkara spp. – Sapotaceae (Souza, 2008) - foram encontrados com marcas de mordidas recentes. O morador que nos acompanhou a este fragmento relatou, o que foi compartilhado por outros moradores, que os guigós também se alimentam deste fruto. Figura 2. Mapa de localização dos guigós no município de Ban- zaê, estado da Bahia, registrados durante o período de realização do presente estudo. Pernoitar no fragmento onde se encontram os guigós, como no caso do fragmento da Fazenda Soturno, mostrou- -se bastante proveitoso quanto à percepção de movimen- tação e vocalização dos grupos. Por volta das 4:00 horas, vocalizações curtas (como aquelas geralmente executadas pelos guigós antes de iniciarem as vocalizações em dueto) já podiam ser ouvidas. E entre 5:00 e 6:00 horas, algumas vocalizações espontâneas (sem indução por playback). No mesmo dia, durante o período da tarde, entre as 15:00 e 16:00 horas, nesse mesmo fragmento, ouvimos mais voca- lizações espontâneas.
Discussão
O fato de um dos pesquisadores ter nascido e residido na região, influenciou sobre maneira na obtenção dos resul- tados. O conhecimento local e o envolvimento com os moradores e as causas ambientais, facilitaram o acesso às propriedades e uma redução de tempo e despesas finan- ceiras pelo contato antecipado com as pessoas mais bem Figura 3. Callicebus barbarabrownae, fotografado na Fazenda Ca- informadas sobre os guigós. Seria proveitoso, sempre que mamu. Imagem: Júnior Monteiro. possível, o trabalho conjunto nas regiões de pesquisa, entre pesquisadores e associações ou movimentos locais envolvi- No Retiro, fragmento onde avistamos um indivíduo, o aces- dos com as questões ambientais atuantes na região. so é difícil, com a trilha beirando um despenhadeiro. Este também foi um dos locais visitados que apresentou o melhor Na região de Banzaê, os guigós ocupam fragmentos de caa- estado de conservação da floresta. Esse fragmento foi visi- tinga arbórea. E para a região, se confirmam os resultados tado posteriormente, contudo, nessa segunda incursão não obtidos por Printes (2011) de que, há maior importância obtivemos resposta acústica ou visual. Na serra da Doroteia da atividade pecuária, em vez de outras atividades agrícolas, foram duas as incursões. A primeira sem respostas, mas na nas propriedades onde os guigós foram localizados. Em segunda, após o acionamento do playback os guigós respon- todos os fragmentos visitados durante a pesquisa, os guigós deram a uma distância aparentemente próxima (menor que foram encontrados nas serras, na parte alta das proprie- dez metros), entretando, devido à composição estrutural da dades, onde geralmente ainda predomina vegetação bem vegetação não conseguimos visualizá-los. No Retiro e na conservada, que devido à dificuldade de acesso, não foram Dorotéia há ainda fragmentos possíveis de abrigarem guigós, suprimidas para dar lugar às pastagens. O sistema agropas- de acordo com relato dos moradores que nos guiaram. Em toril apresenta-se como o fator que maior pressão exerce alguns desses fragmentos foi acionado o playback, entretan- sobre a cobertura vegetal do semi-árido nordestino (Alves to, não obtivemos resposta na ocasião. de Andrade et al., 2005). Neotropical Primates 26(1), September 2020 45
Os guigós provavelmente são indicadores de matas bem podem contribuir para a conservação da espécie na região conservadas (Printes, 2011). Entretanto, mesmo em frag- de Banzaê. mentos de difícil acesso, nas partes altas das serras, às vezes beirando despenhadeiros, nota-se a presença de rebanhos Agradecimentos bovinos e caprinos, estes em menor ocorrência. Os guigós que habitam os fragmentos na Serra da Doroteia são uns Nossos agradecimentos à Associação de Apicultores de dos mais ameaçados registrados neste estudo, pois, além da Banzaê, ao apoio precioso durante a realização da pesquisa presença do gado há uma trilha cortando a serra, onde se em campo, de Lourinho e João de Licero, que nos acompa- realiza evento de motocross. Em uma das reproduções de nharam e dividiram conosco seus conhecimentos adquiri- playback neste fragmento, a resposta veio logo em seguida, dos ao longo da vida no contato com esse ambiente impar mas foi bruscamente interrompida quando os pesquisa- e maravilhoso, que é a caatinga, e à FAPESB, Agência de dores conversaram em tom um pouco elevado durante a Fomento à Pesquisa do Estado da Bahia. espera sob as árvores, e neste dia não houve mais resposta. Referências Talvez, a presença humana para os guigós, seja mais ame- açadora que a presença de outro grupo ou individuo da Alves de Andrade, L. A., Pereira, I. M., Leite, U.T., e Bar- mesma espécie. Reforça essa hipótese o fato de que várias bosa, M. R. V. 2005. Análise da cobertura de duas fi- respostas, em diversos fragmentos, foram interrompidas sionomias de caatinga, com diferentes históricos de uso, depois de certo número de vocalizações e a reprodução do no município de São João do Cariri, Estado da Paraíba. playback por até seis vezes, num intervalo entre a faixa de CERNE 11(3): 253–262. cinco a dez minutos, após a última resposta. Ao se aproxi- Byrne, H., Rylands, A. B., Carneiro, J. C., Alfaro, J. W. marem, os guigós possivelmente avistaram os pesquisadores L., Bertuol, F., da Silva, M. N. F., Messias, M.; Groves, (na maioria das vezes não sendo vistos por estes) o que fez C. P., Mittermeier, R. A., Farias, I., Hrbek, T., Schnei- com que dispersassem. der, H., Sampaio, I., and Boubli, J. P. 2016. Phyloge- netic relationships of the New World titi monkeys (Cal- Apesar da Reserva Indígena Kiriri (Fig. 1) ocupar uma gran- licebus): first appraisal of taxonomy based on molecular de extensão territorial do município de Banzaê (FUNAI, evidence. Frontiers in Zoology 13:10. DOI 10.1186/ 2016) optamos por não fazer nenhuma expedição a estas s12983-016-0142-4 terras, sem antes manter contato com o órgão responsável, Cäsar, C., Byrne, R., Young, R. J., and Zuberbühler K. Fundação Nacional do Índio (FUNAI, 1995). Entretanto, 2012. The alarm call system of wild black-fronted titi em conversas com moradores que frequentam tais áreas, in- monkeys, Callicebus nigrifrons. Behav. Ecol. Sociobiol. v. cluindo um índio da tribo Kiriri, o número de guigós tem 66, n. 5, p. 653–667. aumentado dentro da reserva. Mas a caça ainda é praticada. CPRM (Companhia de Pesquisa de Recursos Minerais). 2005. – Serviço Geológico do Brasil. Projeto Cadastro de Pode-se também observar, ao passar por entre as terras in- Fontes de Abastecimento por Água Subterrânea. Diag- dígenas (a rodovia BA 388, que leva à sede do município, nóstico do Município de Banzaê, Estado da Bahia. Salva- corta a aldeia) o avançado estado de regeneração da vegeta- dor: CPRM/PRODEEM\a. ção em muitas áreas. Este fator pode ter contribuído para Culot, L., Pereira, L. A., Agostini, I., Barreto de Almeida, o aumento da população de guigós. Esses dados, para se- M. A., Cruz Alves, R. S….and Galetti, M. 2019. AT- rem confirmados e aproveitados a favor da preservação da LANTIC-PRIMATES: a dataset of communities and espécie, precisam de estudos e análises concretas. Mesmo, occurrences of primates in the Atlantic Forests of South não tendo conhecimento do status de conservação dos gui- America. Ecology 100(1): 2525. gós, ou ainda sem saber da existência da espécie em sua Freitas, E. B. de. 2010. Levantamento das populações de propriedade, alguns proprietários manifestam interesse em mamíferos e aves em um fragmento de caatinga no alto preservar os fragmentos onde foi confirmada a ocorrência sertão sergipano. Dissertação de Mestrado. Universidade dos guigós, e numa sondagem sobre a criação de RPPNs Federal de Sergipe. São Cristóvão – SE. alguns se mostraram interessados. No entanto vale ressaltar FUNAI, Fundação Nacional do Índio. Art. 4° anexo da que, apesar do desejo de alguns proprietários em preservar instrução normativa no 001/presi, de 29 de novembro estes fragmentos, todos estão ameaçados por motivos diver- de 1995. Disponível em:
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POPULATION DENSITY ESTIMATE FOR THE WHITE-FACED CAPUCHIN MONKEY (CEBUS IMITATOR) IN THE MULTIPLE USE AREA MONTAÑA LA BOTIJA, CHOLUTECA, HONDURAS, AND A RANGE EXTENSION FOR THE SPECIES Eduardo José Pinel Ramos
M.Sc. Biological Sciences, Universidad Nacional Autónoma de Honduras, Cra. 27 a # 67-14, barrio 7 de agosto, Bogotá D.C., e-mail:
Abstract
Honduras is one of the Neotropical countries with the least amount of information available regarding the conservation status of its wild primate species. Understanding the real conservation status of these species is relevant, since they are of great importance for ecosystem dynamics due to the diverse ecological services they provide. However, there are many threats that endanger the conservation of these species in the country such as deforestation, illegal hunting, and illegal wild- life trafficking. The present research is the first official registration of the Central American white-faced capuchin monkey (Cebus imitator) for the Pacific slope in southern Honduras, increasing the range of its known distribution in the country. A preliminary population density estimate of the capuchin monkey was performed in the Multiple Use Area Montaña La Botija using the line transect method, resulting in a population density of 1.04 groups/km² and 4.96 ind/km² in the studied area. These results provide us with a first look at an isolated primate population that has never been described before and demonstrate the need to develop long-term studies to better understand the population dynamics, ecology, and behaviour, for this group in the zone.
Key Words: Distribution, population density, Cebus imitator, Capuchin monkeys, Honduras.
Resumen
Honduras es uno de los países del Neotrópico en donde menos información se tiene acerca del estado de conservación de sus especies de primates silvestres. El conocimiento del estado real de conservación de estas especies es relevante ya que son de gran importancia para las dinámicas de los ecosistemas debido a los diversos servicios ecológicos que ofrecen. Sin embargo, en el país se presentan amenazas que ponen en riesgo la conservación de estas especies como son: la deforestación del bosque, la cacería y el tráfico ilegal de especies silvestres. En esta investigación se hace el primer registro oficial de monos capuchinos cara blanca (Cebus imitator) para la vertiente del Pacifico en el sur del país, de esta forma se amplía su rango de distribución para Honduras. Se realizó una estimación preliminar de las densidades poblacionales de esta especie en el Área de Usos Múltiples Montaña La Botija, utilizando el método de transectos lineales, dando como resultado una densidad poblacional de monos capuchinos de 1.04 grupos/km² y 4.96 ind/km² en el área de estudio. Estos resultados nos dan un acercamiento a una población de primates aislada de la que no se tenía ningún registro previo y nos muestran la necesidad de realizar estudios a largo plazo con esta población para poder entender de mejor manera las dinámicas poblacionales, ecología y comportamiento de este grupo en la zona.
Palabras Clave: Distribución, densidad poblacional, Cebus imitator, monos capuchinos, Honduras.
Introduction Honduras has high overall biodiversity due to its topogra- phy and its location in a tropical zone, among other factors Neotropical primate species are of great importance in (SERNA, 2001). Currently three wild primate species are tropical ecosystem dynamics, since they act as seed dis- reported in the country: the spider monkey Ateles geoffroyi persers, pollinators and are an important part of the food (Kuhl, 1820), the capuchin monkey Cebus imitator (Thom- chain as pray and predators (de la Torre, 2000). They are as, 1903), and the howler monkey Alouatta palliata (Gray, primarily arboreal with a wide variety of diets (Chapman 1849). However, none of these species are officially regis- and Chapman, 1990) and complex social systems (Kin- tered in the southern region of Honduras. Reid (2009) in- zey and Cunningham, 1994). They also encompass wide dicates the presence of these species in most of the country diversity in body size and color (Robinson and Redford, in the distribution maps in the publication “A field guide to 1984). While the biodiversity of Neotropical primates is the Mammals of Central America And Southeast Mexico,” highest in tropical rainforests, some species prefer decidu- however these are very general maps without mention of ous, gallery or montane forests at more than 2,000 m a.s.l. any specific locality where these species might be present (Chivers, 1982). in Honduras. 48 Neotropical Primates 26(1), September 2020
Some of the main factors that have a negative impact on “El Tamarindo” with 2.2 km (13°17′39.5″ N 86°48′42.3″ global biodiversity are: habitat loss (Brooks et al., 2002), W), “Los Mogotes” with 1.8 km (13°17′08″ N 86°44′37″ competition with invasive species (Clavero and Gar- W) and the “Montaña Oscura” transect with 2.5 km cia-Berthou, 2005), host-pathogen interactions (Roche (13°17′54.5″ N 86°44′54.3″ W) (Fig. 1). A total of 8.5 et al., 2012), climate change (Alan Pounds et al., 2006) linear km of sampling transects were created, located be- and illegal hunting (Grayson, 2001); with hunting the tween 500 to 1,200 m a.s.l. main cause attributed to the extinction of large mammals and birds (Peres, 2000; Barnosky et al., 2004; Suarez et al., 2009). All of these factors are currently present in most of the protected areas in Honduras (Secaria, 2013), one of the Neotropical countries with the least amount of information available regarding the conservation sta- tus of its wild primates and with little research published. Two doctoral theses provide some of the most relevant data available for wild primates in Honduras. The first one, by Buckley (1983) described feeding behavior, so- cial behavior, and ecology of the white-faced capuchin monkey (Cebus imitator) near the city of Trujillo, in the north of Honduras. Thesecond doctoral thesis, by Hines (2005), the first study on spider monkeys (Ateles geoffroyi) in Honduras, focused on the ecology and taxonomy of Figure 1. Study area and the 4 transects used: (1) transect El Ojo- spider monkeys at the Pico Bonito National Park in the chal, (2) transect Montaña Oscura, (3) transect Los Mogotes, (4) department of Atlántida. Additionally, there is a note transect El Tamarindo. about an albino spider monkey in captivity in the city of Catacamas at the department of Olancho, Honduras Data Collection (Espinal et al., 2016). Data collection occurred during June to December 2011. It consisted of monthly field trips with an average dura- Given the current conservation concerns and lack of knowl- tion of 10 days, for a total of 65 days of field work. The edge about Honduran primates, it is important to develop duration of each trip varied based mainly on the weather long term studies to know and learn more about the ecol- conditions of the study area. ogy, behavior, distribution, and conservation status of the existing primate species in the country. The main goal for To estimate the population density of Cebus imitator, the this research was to verify the presence and estimate the line transect method was used, following the proposed population density of white-faced capuchin monkeys (Ce- guidelines by NRC (1981) and Peres (1999b). This meth- bus imitator) in the Multiple Use Area “Montaña La Botija” od has been widely applied during the last three decades (AUMLB), Honduras. to quantify primates’ population abundance in tropical forests (Peres, 1999b). The four transects were randomly Materials and Methods walked, one each day and not repeating the same tran- sect on two consecutive days, an average of three times Study area each transect per field trip. For round trip walks on the The AUMLB was declared a protectedarea in 2005. It is transect, the travel in each direction was considered as in- located in the department of Choluteca, in the southern dependent. The outward walks weredone from 06:00 to region of the Pacific slope of Honduras (ANED, 2009). In 10:00 hours, and the return walks were done from 14:00 order to select the study area, interviews were conducted to 18:00 hours, waiting approximately 3 hours at the end with the local residents and satellite images of the area were of the transect, usually at midday when the primates are studied to determine the place with the most likely con- less active, time enough for the animals to redistribute on ditions to encounter the species (less human intervention, the space (Wallace et al., 1998; Peres, 1999b; Quinten, greater amount of forests, and where the locals mentioned 2016). It is also important to mention that there was greater probability to find it). The chosen place was “La never more than one encounter in a given transect on the Montaña del Ojochal” located in the dry tropical forest same day. life zone (Holdridge, 1967). The annual rainfall is between 1,000 and 2,000 mm and temperatures are above 24 °C When a group of the studied species was detected, obser- during the whole year (Holdridge, 1967). This area is lo- vations were made during a standardized amount of time cated between 450 and 900 m a.s.l. (ANED, 2009). (ten to fifteen minutes). Guidelines in the methodology included that the observer should remain on the census A preliminary six-day trip was carried out, to prepare and transect path and not follow the animals outside the tran- establish the transects inside the study area: “El Ojochal” sect line (Peres, 1999b). When possible, the following in- with a length of 2 km (13°17′47.6″ N 86°44′35.3″ W), formation was registered for the studied species during the Neotropical Primates 26(1), September 2020 49 census walks: time and location in the transect, location are highly opportunistic foragers, capable of manipulating of the sighted population (angle calculated using a field a wide range of materials and substrates whether to feed, compass and the perpendicular distance from the transect move or defend themselves since they have great skills with to the first sighted individual), group composition by age their hands (Rose, 1994). Their varied diet allows them to and sex, and opportunistic observations (species of feeding make changes in their feeding resources in different parts trees utilized). of the year when, for example, some fruits are scarce or are not in season (Chapman and Fedigan 1990). This flexibil- Thanks to these censuses it was possible to determine the ity reduces competition with other arboreal mammals like number of individuals per transect area and subsequent- spider monkeys, squirrel monkeys, coatis, anteaters, and ly for the study area. It was also possible to estimate the even some birds. The capuchin monkey uses all the forest number of groups of existing primates, as well as the com- levels and travels on the ground to cross open areas, drink position and quantity of individuals in each of them. Ad- water and forage. Their active hours start early in the day ditionally, maturity stage was categorized as follows: adult and they are more active during the morning and afternoon (large individuals with fully developed sexual characteris- (Reid, 2009). tics), sub-adult (same size as the adult but with a slimmer body structure), juvenile (medium individual with less Results developed sexual characteristics), infant (small individual who spent most of its time being carried by an adult). The presence of the capuchin monkey (Cebus imitator) was registered in the Pacific slope of Honduras through several In addition to data collected to estimate capuchin popula- encounters in three of the four transects used within the tion density, samples were collected from all the trees for study area (El Ojochal, El Tamarindo and Los Mogotes). approximately 5 m from each side of the transect with a During these encounters, pictures and videos of different circumference larger than 15 cm at breast height; samples individuals were taken for identification purposes, as well with flower or fruit could classified more precisely, however as to provide evidence for the presence of the species in the due to factors such as crown height or because a tree was zone (Fig. 2). not flowering or fruiting at the time, this was not always possible. Collected samples were identified by profession- als at the Herbarium of the Biology Department at the Universidad Nacional Autónoma de Honduras.
Study species Cebus imitator (Thomas 1903) The IUCN places this species in the Least Concern cate- gory (LC) (Rylands et al., 2013). CITES places it in the II appendix for Honduras (many populations are threat- ened by deforestation and illegal trafficking). This species belongs to Cebidae and is distributed in Central America from northwest Honduras to Panama, and from sea level to 1,500m (Boubli et al., 2012; Rylands et al., 2013). Its fur is black, except the face and ears, the sides of the neck, the shoulders, the chest, and the upper part of the arms, which are white-yellowish. It has a black prehensile tail (Emmons Figure 2. Photograph of an adult male (AM) in the transect El and Feer, 1997). White-faced capuchins live in large mul- Ojochal. ti-female, multi-male troops of up to 40 individuals, with female philopatry and male dispersal to other groups as ju- Each transect was walked 34 times during the study, for a veniles (Oppenheimer, 1968; Freese, 1978; Fedigan, 1993). total of 28 km and more than 800 hours of work, resulting Within the groups’ dominance levels, both sexes present a in 142 minutes of visual contact with the species and more linear hierarchy (Perry, 1995; Jack and Fedigan, 2006). In than 20 minutes of video recorded for different individu- females, this hierarchy, is due to matrilineal kinship and als. From these walks there were a total of nine encounters coalitions, while in males is mainly, due to intrasexual com- with capuchin monkeys and a total of 43 individuals reg- petition (Perry, 1995; Perry, 1998; Jack, 2003). Capuchins istered, with an average group size of 4.7 ind/group (3-9 are territorial animals with a consistent home range that range). Due to the low number of encounters it was not sometimes can overlap with other groups. They are omniv- possible to use the software Distance to run the population orous and have one of the most varied diet among the Neo- density analysis. However, it was possible to estimate the tropical primates, feeding on vegetable matter (fruits, flow- individual and group density per transect and for the whole ers, shoots, nuts), insects and small vertebrates (Chapman study area using the formulas established by the National and Fedigan, 1990; Eisenberg and Redford, 1999). They Research Council (NRC, 1981; Table 1). 50 Neotropical Primates 26(1), September 2020
Table 1. Population density of Cebus imitator on each of the transects used during the research.
Transect Group density Individual Density Variance Confidence limits Accuracy % (groups/km2) (individuals/km2) by 95 %
El Ojochal 3.06 14.38 1.8663 0.6535 14.00 El Tamarindo 1.12 5.27 1.2916 0.4523 9.046 Los Mogotes 0.46 2.16 0.3429 0.1200 12 Montaña Oscura 0 0 ______Total area 1.04 4.96 1.4987 0.2951 6.1787
It was not always possible to identify sex due to the an- by the Tinto riverbank. Thisis one of the best-preserved imals’ fast movement, low visibility because of the forest forest patches in the area, although it has been recently af- cover, and the field’s irregular topography. However, it was fected by human activity. possible to differentiate stage of maturity, based on size (30 adults, 10 sub-adults and 3 juveniles). This research had a total of nine focal encounters with Cebus imitator in the whole research area, which is a low Plants identified in the forest included 689 individual trees, number of encounters in comparison with some other which were distributed in 62 different species pertaining studies of the species (Chapman et al.,, 1988; Estrada and to 32 families, with Lysiloma auritum the most abundant Coates-Estrada, 1996; Timock and Vaughan, 2002; Tins- species (133 individuals or 19.3 %), followed by Bursera ley Johnson et al., 2020), but similar to the ones reported simaruba and Neomillspaughia paniculata (52 individu- in the wildlife refugee centre “Rio Escalante-Chococente”, als or 7 % each), Quercus sp. (53 individuals or 7 %) and in the south of Nicaragua (Williams-Guillén et al., 2013), Brosimum alicastrum (41 individuals or 5 %). Some of the although these authors mention their study was possibly registered plants were used as food by the capuchin mon- an under-registration of encounters for the species in this keys during the study, including the fruit, the flower or less area. Estimations obtained from a low number of encoun- commonly, the leaf (Table 2). ters must be cautiously interpreted (Plumtre, 2000; Gon- zales-Solis et al., 2001), but the data are especially relevant Table 2. Plant species used as food by Cebus imitator inside the when there is no other information available for the species study area. in the study area.
Family Species Item Encounters with capuchin monkeys occurred in three out Anacardiaceae Spondias purpurea Fruit of the four established transects for the study. The tran- sect “Montaña Oscura” was the only one without any en- Apocynaceae Tabernaemontana Fruit counters with the species, despite being the most extensive donnell-smithii transect in length (Fig. 1) with the same number of walks Burseraceae Bursera simaruba Fruit performed as in the other ones. This maybe attributed to Fabaceae Acacia deamii Young leaves many factors, including its elevation from 800 to 1,040 Fabaceae Inga vera Fruit m.a.s.l., which in the study area corresponds to a shift in Malpighiaceae Byrsonima crassifolia Fruit the dominant plant species to Quercus sp. and Pinus oocar- pa. This transect was also the one closest to a main road, Malvaceae Guazuma ulmifolia Flower with three communities and an active mine (during data Moraceae Brosimum alicastrum Fruit collection) where cars and the mine’s engines produced Moraceae Ficus cotinifolia Fruit loud noises that could have affected the monkeys’ presence Muntingiaceae Muntingia calabura Fruit or the possibility to detect them.
Rubiaceae Chiococca alba Flower A population density of 1.04 groups/km² and 4.96 ind/ km² was estimated for AUMLB. From 142 minutes Discussion of visual contact and more than 20 minutes of video re- corded, it was possible to differentiate 6 individuals (2 The presence ofCebus imitator inside AUMLB was con- adult males, 1 adult female, 2 subadult males and 1 sub- firmed, the first official registration ofthis or any non-hu- adult female), using scars and physical characteristics as man primate species in the Honduran Pacific slope in the a reference. The six differentiated individuals were from southern part of the country. The capuchin monkey, one the same group, subjects of several encounters along the of the three primate species reported in Honduras, is the Ojochal transect. During the encounters in the Tamarindo only one present in the study area. It is distributed in El and Mogotes transects, it wasn’t possible to differentiate the Cañon del Ojochal, a remnant of tropical dry forest located individuals, so it could not be determined if this was the Neotropical Primates 26(1), September 2020 51 same group from the Ojochal transect or a different one. ranching or agriculture for annual crops of corn or beans. However, based on the field conditions and the distances The existence of these crops has created a conflict between between transects, I believe it is possible there are at least monkeys and humans, as local people express they are two different groups in the study area. No capuchin in- experiencing economic losses because of the damage the fants were observed during the walks, but this could be monkeys cause to their crops, mainly in corn fields. An- explained by the timid and evasive behavior of the species other factor is forest cover loss because of fires during dry in the presence of the researcher, making direct observa- seasons. In addition, local people are not aware of the im- tions difficult for all individuals in the group. Another portance of this species on the ecosystem, and finally, there factor could be the limited experience of the researcher at is no protection from the government towards this or other the time of the development of the study, as well as the species living within the limits of the country’s protected possibility of birth seasonality patterns of the species in the areas (Secaria, 2013). study area (Di Bitetti and Janson, 2000), or long interbirth intervals like the ones reported for this species in Costa Food resource availability is a determining factor for pri- Rica (Fedigan and Rose, 1995). This situation could also mate abundance; deforestation is the most significant serve as a wake-up call, since the absence of infants could problem capuchins face in AUMLA (Terborgh, 1983; be a symptom of the population’s poor health, bringing up Balcomb et al., 2000; Stevenson, 2001; 2016). Capuchin serious doubts about the likelihood of continuity of the monkeys are susceptible to habitat loss and tend to recov- species in the zone. er more slowly compared with other primate species like the howler monkey (Roncancio and Gomez-Pozada, 2009; For a better understanding of the current situation of the Amato et al., 2014). This is related to their diet, since species in the study area, the results here were compared capuchin monkeys need a greater area of forest to fulfill with population densities obtained for Cebus imitator in feeding needs, and in periods of fruit scarcity, are forced to Panama, Costa Rica, and Nicaragua (Table 3). travel greater distances to findfood, different from howler monkeys that can survive on a folivorous diet (Milton and Table 3. Capuchin monkey population density comparison Fedigan, 2004). across studies. It is probable that the presence of the Cebus imitator in the Number of Location Source area is a result of the existence of an old biological corridor individuals that connected the Honduran and the Nicaraguan “Mos- (ind/km2) quitia” with the south of Honduras and went all the way 12.3 +/– 7 Punta Leona Private Timock and around the Coco o Segovia River. This biological corridor Wildlife Refuge, Vaughan, 2002 was also used by other species that local people have men- Costa Rica tioned seeing in the area a long time ago, such as the jaguar 17.73 – 32.57 Santa Rosa National Chapman et al., (Panthera onca), the howler monkey (Aloutta palliata), and Park, Costa Rica 1988 the spider monkey (Ateles geoffroyi), among other species 1.08 Coiba Island Mendez-Carvajal, (Marineros and Martinez, 1998) that are no longer present National Park, 2012 in the area. Republic of Panama 31 +/– 26 Manuel Antonio Estrada et al., The continuous forest that once allowed for the movement National Park, 2006 of capuchin monkeys and other species between the north Costa Rica and south of Honduras has been logged and fragmented to 34.47 Santa Rosa, Costa DeGama- build up cities, roads, agriculture fields and cattle ranching, Rica Blanchet and leaving scattered patches of forests in the whole region, and Fedigan, 2006 limiting the flowof species between the two slopes (Fig. 3). This impact is so strong that the closest registered pop- 11 Southwestern Williams-Guillén Nicaragua et al., 2013 ulation of capuchin monkeys according to Marineros and Martinez (1998) can be found approximately 89 km away 36.24 Taboga Forest, Tinsley Johnson Costa Rica et al., 2020 in the Valle de Jamastran in the department of El Paraiso (Figure 3); these two populations are completely isolated 4.96 Multiple Use Area Present study from each other, with cities and towns between them. Fig- “Montaña La Botija”, Honduras ure 3 includes other registered locations of known popula- tions of Cebus imitator at the moment in Honduras. Ta- ble 4 shows the corresponding localities and coordinates, Factors affecting the population density of capuchin mon- as well as sources including books, management plans for keys in the study area include: selective logging, and the protected areas, a doctoral thesis, and the author’s personal transformation of forest into grassland for extensive cattle observations. 52 Neotropical Primates 26(1), September 2020
Figure 3. Map of the Atlantic and Pacific slopes and their connection through the Coco o Segovia River.
Table 4. Localities and coordinates of other populations of Cebus imitator in Honduras.
Number Locations Coordinates Source
1 Trujillo Mangroves 15°55’56.34”N Buckley, 1983 85°55’0.24”W 2 Jamastran Valley 13°59’22.26”N Marineros and Martinez, 1998 86°27’39.50”W 3 Laguna de los Micos 15°48’15.40”N Marineros and Martinez, 1998 87°36’20.12”W 4 Capiro y Calentura National Park 15°52’19.51”N Marineros and Martinez, 1998 85°56’27.94”W 5 Pisijire village, Olancho 15°10’17.93”N Marineros and Martinez, 1998 85°26’49.37”W 6 Krausirpi village, Gracias a Dios 15° 2’39.05”N Marineros and Martinez, 1998 84°52’26.76”W 7 Texiguat Wildlife Refuge 15°27’44.29”N Marineros and Martinez, 1998 87°16’53.72”W 8 Laguna de Guaymoreto 15°57’58.60”N Marineros and Martinez, 1998 85°51’35.92”W 9 Cusuco National Park 15°33’46.39”N Marineros and Martinez, 1998 88°18’12.44”W 10 Sierra de Agalta National Park 14°58’1.92”N Marineros and Martinez, 1998 85°51’47.66”W 11 Jeannette Kawas National Park 15°49’6.54”N PROLANSATE, 2004 87°22’12.32”W 12 Punta Izopo National Park 15°49’27.38”N PROLANSATE, 2004 87°21’4.75”W 13 Biosfera del Río Plátano 15°27’4.89”N Zambrano, 2008 84°48’50.08”W 14 La Muralla Wildlife Refuge 15° 4’58.16”N CEAH, 2010 86°45’22.03”W 15 Cuero y Salado Wildlife Refuge 15°46’45.11”N Portillo and Carrasco, 2012 87° 8’27.37”W 16 Pico Bonito National Park 15°36’59.03”N Carrasco et al., 2013 86°51’42.77”W Neotropical Primates 26(1), September 2020 53
Number Locations Coordinates Source
17 Botaderos National Park 15°26’3.02”N Guillen and Guillen, 2013 86° 4’50.36”W 18 San Antonio village, Cortés 15°45’18.54”N Personal observation 88° 2’47.38”W 19 Patuca National Park 14°17’54.14”N Personal observation 85°13’53.01”W 20 Santiago village, Atlantida 15°39’4.09”N Personal observation 87°37’51.94”W 21 Nombre de Dios National Park 15°47’49.16”N Personal observation 86°32’40.32”W 22 Pico Pijol National Park 15°10’26.09”N Mioñes et al., 2018 87°34’25.26”W 23 Montaña La Botija 13°17’38.03”N Current study Multiple Use Area 86°44’41.81”W
These preliminary results point to a clear need to continue Balcomb, S. R., Chapman, C. A. and Wrangham, R. W. the study of this capuchin monkey population (Cebus im- 2000. Relationship between chimpanzee (Pan troglodytes) itator) in southern Honduras in order to determine with density and large, fleshy-fruit tree density: conservation greater certainty its current conservation status. It is also implications. Am. J. Primatol. 51:197–203. necessary to search for closer populations to this study area Barnosky, A. D., Koch, P. L., Feranec, R. S., Wing, S. L. to better understand migration dynamics as this capuchin and Shabel, A. B. 2004. Assessing the causes of Late Pleis- monkey population, the only one reported up to this point tocene extinctions on the continents. Science. 306(5693): in this region of the country, is in real danger of disappear- 70-75. ing from the area. Boubli, J. P., Rylands, A. B., Farias, I. P., Alfaro, M. E. and Alfaro, J. L. 2012. Cebus Phylogenetic Relationships: A Acknowledgments Preliminary Reassessment of the Diversity of the Untuft- ed Capuchin Monkeys. Am. J. Primatol. 74(4): 381–393. To Enrich the World Honduras for supporting me finan- doi:10.1002/ajp.21998 cially and logistically during all the field work. To my Brooks, T. M., Mittermeier, R. A., Mittermeier, C. G., teachers Gustavo Cruz, Karla Cantarero and Gerardo Bor- Da Fonseca, G. A. B., Rylands, A. B., Konstant, W. R., jas for their advice and instruction during this research. T Flick, P., Pilgrim, J., Oldfield, S., Magin, G. and Hilton‐ o Klaus Wiese, Julio Mérida, Hermes Vega and David Es- Taylor, C. 2002. Habitat Loss and Extinction in the pinoza for helping me with the identification of the plant Hotspots of Biodiversity. Conserv. Biol. 16: 909–923. species and their advice during manuscript preparation, to doi:x10.1046/j.1523-1739.2002.00530. Angélica Hernández for the translation of the manuscript, Buckley, J. S. 1983. The Feeding Behavior, Social Behavior, and finally to Jessica Lynch for the recommendations and and Ecology of the White-Faced Monkey, Cebus capuci- comments on the previous versions of the manuscript. nus at Trujillo, Northern Honduras, Central America, Ph.D. thesis, University of Texas at Austin. References Carrasco, J. C., Secaira, E., and Lara, K. 2013. Plan de Conservación del Parque Nacional Pico Bonito: Basado Alan Pounds, J., Bustamante, M., Coloma, L., L. A., Con- en Análisis de Amenazas, Situación y del Impacto del suegra, J. A., Fogden, M. P. L., Foster, P. N., La Marca, Cambio Climático, y Definición de Metas y Estrategias. E., K. L. Masters, Merino-Viteri, A., R. Puschendorf, ICF, USAID ProParque y FUPNAPIB. 54 pp. Ron, S. R., A. Sánchez-Azofeifa, C. J. Still, and Young, CEAH. 2010. Plan de Manejo Refugio de Vida Silvestre B. E. 2006. Widespread amphibian extinctions La Muralla 2011 – 2015. Instituto Nacional de Con- from epidemic disease driven by global warming. Nature. servación y Desarrollo Forestal, Áreas Protegidas y Vida 439: 161–167. https://doi.org/10.1038/nature04246 Silvestre ICF. 252 pp. Amato, K. R., Leigh, S. R., Kent, A., Mackie, R. I., Yeo- Chapman, C. A. and Chapman, L. J. 1990. Dietary var- man, C. J., Stumpf, R. M., Wilson, B. A., Nelson, K. E., iability in primate populations. Primates. 31: 121–128. White, B. A. and Garber, P. A. (2014). The Gut Microbi- https://doi.org/10.1007/BF02381035 ota Appears to Compensate for Seasonal Diet Variation in Chapman. C., L. Fedigan, and L. Fedigan. 1988. A com- the Wild Black Howler Monkey (Alouatta pigra). Microb. parison of transect methods of estimating population Ecol. 69(2): 434–443. doi:10.1007/s00248-014-0554-7 densities of Costa Rican primates. Brenesia 30: 6780. ANED, C. 2009. Plan de manejo del Área de usos múlti- Chapman C. A. and Fedigan L. M. 1990. Dietary Differ- ples La Botija. Sin publicar.136 p. ences between Neighboring Cebus capucinus Groups: 54 Neotropical Primates 26(1), September 2020
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REDUCCIÓN EN LA DENSIDAD POBLACIONAL DEL TITI GRIS (SAGUINUS LEUCOPUS) EN EL ORIENTE DE CALDAS, COLOMBIA Néstor Roncancio D.1, Jennifer Branch B.1, Oscar Felipe Moreno-Mancilla1,3, María Isabel Blanco N.1, Oscar Ospina H.1 and Lina Marcela Guzmán2
1Corporación Autónoma Regional de Caldas – Corpocaldas 2Universidad Nacional de Colombia 3 Fundación BIEVEP. Grupo de Investigación Biología Evolutiva y Epistemológica. Correo electrónico para correspondencia: [email protected]
Resumen
El monitoreo de parámetros poblacionales es básico para formular y adaptar las estrategias de manejo de la vida silvestre. En el oriente de Caldas, en el marco de alianzas público-privadas, se han venido implementando estrategias de manejo y moni- toreo de titi gris (Saguinus leucopus) como especie prioritaria para la región. Esta especie está En Peligro debido a la reducción y fragmentación de su hábitat y a la cacería por comercio. Durante el 2015 se llevaron a cabo estimaciones de densidad poblacional para actualizar el diagnóstico del estado de conservación del primate y compararlo con estimaciones previas de 2006 y 2008. En este muestreo, las densidades encontradas en el oriente de Caldas estuvieron entre 14 y 109 ind/ km2. Para dos de las cuatro localidades en donde se hizo un segundo muestreo se presentaron reducciones del 61 y 70 % en com- paración con el 2008. Es altamente probable que estas disminuciones estén asociadas a cacería por comercio producto del aumento de la accesibilidad por los cambios sociopolíticos de la región.
Palabras Clave: Monitoreo efectivo, cambios sociopolíticos, densidad poblacional, titi gris
Abstract
Monitoring of population parameters is basic to plan and adapt the management strategies of wildlife. In the east of Caldas region, in a framework of the public-private alliances, they have implemented management strategies and monitoring of white-footed tamarin (Saguinus leucopus) as a priority species to this region. This species is in Endangered due to habitat reduction and fragmentation and pet trade. During 2015 we carried out a population density estimation to get current the diagnosis of conservation status of the primate and to compare with previous estimates in 2006 and 2008. In this sampling, the population densities were between 14 and 109 ind/km2. In two out of the four localities that were sampled a second time, there were reductions of 61 and 70 % comapred with 2008. It is highly probable that these decreases are associated with the pet trade as a result of the increase in accessibility to the area driven by the socio-political changes in the region.
Key Words: Effective monitoring, socio-political change, population density reduction, White-footed tamarin
Introducción obstante, una estimación de la densidad poblacional de una especie es preferible dado que este parámetro refleja El manejo efectivo de áreas protegidas y otras estrategias de la relación que hay entre la población y el área que ocupa conservación depende de la aplicación de acciones de ma- (Witmer, 2005). Por otro lado, dado que los parámetros nejo efectivas. Definir las acciones de manejo apropiadas demográficos como la densidad poblacional son dinámicos requiere de información confiable derivada de la evidencia espacial y temporalmente, su monitoreo efectivo es esencial científica además de la experiencia que los administradores para detectar sus tendencias y las relaciones que tienen con adquieren en su ejercicio (Possingham et al., 2001; Pullin y los factores que los modulan y de esta forma poder adap- Knight, 2005; Nichols y Williams, 2006). En el caso de las tar las acciones de manejo (Gibbs et al, 1998; Gibbs et al, especies amenazadas o de las que son usadas como elemen- 1999; Legg y Nagy, 2006; Lyons et al., 2008; Lindenmayer tos sustitutos de la diversidad en un paisaje para orientar et al., 2011). El monitoreo en sentido amplio se entien- acciones de manejo, es necesario hacer diagnósticos cuan- de como cualquier medida repetida de un fenómeno. Sin titativos de su estado de conservación (Yoccoz et al., 2001; embargo, en conservación es necesario que quede explícito Gielh et al., 2017). que un monitoreo efectivo, debe lograr en los estimadores la precisión necesaria para detectar cambios si los hay (po- Un paso inicial para conocer el estado de una población tencia estadística) (Elzinga, 2001; Sutherland, 2006; Field es hacer una estimación empírica de su abundancia, no et al., 2007; Marsh y Trenham, 2008). Neotropical Primates 26(1), September 2020 57
Saguinus leucopus es una especie En Peligro (Morales et al., 2008 en al menos seis sitios diferentes, encontrando den- 2008) dado que su distribución se encuentra en una zona sidades que varían entre 54 y 149 ind/ km2 (Roncancio con alto impacto por actividades humanas, que generan un et al., 2011; Sanchez-Londoño, 2013). Sin embargo, no continuo proceso de reducción y fragmentación de hábitat. se han hecho replicas temporales que permitan evaluar la El área de distribución original de la especie, que cubría respuesta de estas poblaciones a la reducción y fragmen- aproximadamente 48,000 km2, ha perdido más del 40 % de tación de su hábitat y otras amenazas como la presión de hábitat disponible (Roncancio et al., 2013) y actualmen- cacería en diferentes escenarios. Por lo tanto, este trabajo, te está conformada por cultivos (23 %), pastos (22 %), y además de evaluar nuevos sitios para la especie en el orien- coberturas vegetales naturales (32 %). Las coberturas na- te de Caldas, tuvo como objetivo evaluar el cambio de la turales incluyen principalmente Bosque Denso con frag- densidad población del primate en sitios ya muestreados. mentos de entre menos de 0.1 a 300 km2 hasta 6,000 km2 (media = 60 km2 ± DE 1640), de formas irregulares (Índice Métodos Medio de Forma = 1.8), y con conectividad media (Índice de yuxtaposición - interpersión = 52) (análisis hechos en Area de estudio este trabajo con la capa de coberturas IDEAM et al. 2012). El oriente de Caldas en jurisdicción de los municipios Particularmente en el oriente de Caldas (Municipios de de La Dorada, Norcasia, Victoria y Samaná es el área del Samaná, Norcasia, Victoria y La Dorada) en un territorio departamento en donde se encuentra parte de la distri- de 2,100 km2 los bosques y áreas seminaturales han pasado bución de Saguinus leucopus (Roncancio, 2013). Algunas desde el 2002 de cubrir 845 km2 a 757 km2 en 2009 y a de estas áreas se encuentran bajo una figura de protección 2012 cobijaban poco más de 630 km2 (30.3 %), para una mientras que otras, producto de las dinámicas sociales y pérdida de más de 20,000 ha en 10 años. Las coberturas de uso del suelo de la región, aún son áreas de conserva- vegetales naturales a 2012 en el oriente de Caldas estaban ción o, en ellas se han dado procesos de regeneración. Las representadas por 402 parches de aproximadamente 158 estimaciones de la densidad poblacional de S. leucopus se ha en promedio (DE = 322) con formas irregulares (mayor llevaron a cabo en seis localidades que difieren en tama- efecto de borde) (IMF = 3.36) y son en su mayoría vegeta- ño, forma, distancia de aislamiento, altitud y cobertura ción secundaria o en transición (52 %) y bosques de galería vegetal, representando toda la variación que presenta el (24 %) (análisis hechos en este trabajo con la capa de cober- paisaje del oriente de Caldas dentro del rango altitudinal turas IDEAM et al. 2012). preferido por la especie (0 – 1,100 m). Las seis localida- des evaluadas fueron, Distrito de Manejo Integrado (DMI) Por otro lado, esta especie es el primer primate y segun- Charca de Guarinocito (5°20’13’’N; -74°44’06’’W), Re- do mamífero más traficado de Colombia (MADS, 2012). serva Natural de la Sociedad Civil (RNSC) de Río Manso En ese sentido se han reconocido, bajo criterios de severi- (5°40’40’’N; -74°46’26’’W), La Habana (Finca Pozo Re- dad, proporción de área de distribución afectada y rever- dondo) (5°38’48’’N; -74°45’58’’W) y la RNSC Venecia sibilidad, a la reducción y fragmentación del hábitat y a la – Jagual (5°38’21’’N; -74°50’21’’W), Embalse Amaní, di- cacería para comercio como las dos principales amenazas vidida en seis sitios (Carrizales, Los Mangos, Sasaima, Ca- para la conservación de esta especie con una ponderación ñaveral, La Clara y el trasvase del Río Manso) (5°33’17’’N; de muy alta y alta respectivamente (Franco y Roncancio, -74°53’38’’) y el sector Bella Vista – Delgaditas – Guarinó 2011). En el oriente de Caldas se han hecho estimacio- (5°22’28’’N; -74°56’20’’) (Tabla 1, Fig. 1). nes de densidad poblacional de tití gris entre el 2005 y el
Tabla 1. Localidades en donde se estimó la densidad poblacional de Saguinus leucopus.
Localidad Área (ha) Altitud (m s.n.m.) Cobertura DMI Charca de Guarinocito 21 200 Bosques de galería
RNSC Río Manso 313 220 -340 Bosque denso
La Habana 52 200 - 250 Bosque denso
RNSC Venecia – Jagual 100 380 -420 Bosque denso y bosque de galería Amaní 2552 250 - 850 Bosque denso y bosque fragmentado Bella Vista – Delgaditas – 431 440 -1,030 Bosque denso y bosque Guarinó de galería 58 Neotropical Primates 26(1), September 2020
Los muestreos se llevaron a cabo desde las 8:00 hasta las 12:00 h y de las 14:00 hasta las 17:00 h y fueron ejecutados por tres observadores recorriendo simultáneamente un tran- secto cada uno. Para garantizar que durante el recorrido de cada transecto se mantuviera constante la probabilidad de detección se fijó lavelocidad de desplazamiento en 500 me- tros por hora. Cada vez que fue ubicado un grupo se perma- neció no más de 15 minutos (Peres, 1999) intentando hacer el conteo completo del grupo. Los muestreos se llevaron a cabo en la RNSC de Río Manso entre el 3 de febrero y el 13 de marzo. En la Habana entre el 15 de marzo y el 21 de abril y entre el 5 y 12 de junio. En la RNSC Venecia se hicieron entre el 6 de abril y el 21 de mayo. En Amaní entre el 14 de julio y el 15 de septiembre, y, en Bella Vista – Guarinó y Del- gaditas entre el 19 de septiembre y el 31 de octubre de 2015.
DMI Charca de Guarinocito El muestreo se llevó a cabo entre el 30 de enero y el 2 de febrero de 2015. Dado que el DMI Charca de Guarino- cito es un fragmento pequeño (21 ha) y alargado (permite tener una visual de todo el ancho) no se usó el método de muestreo por distancia con transectos lineales para hacer la Figura 1. Area de estudio, en donde se indican las localidades en estimación de la densidad; se hizo un censo (conteo com- donde se llevó a cabo la segunda replica temporal en el muestreo pleto), dado que las condiciones de sitio permiten satisfacer para estimar la densidad de Saguinus leucopus (círculos negros). los supuestos de que se puede evaluar toda el área de interés y contar todos los objetos buscados. Cuatro profesionales Toma de datos hicieron búsqueda y seguimiento de grupos entre las 6:00 y RNSC Río Manso, La Habana, RNSC Venecia-Jagual, 18:00 hasta confirmar la estructura y composición de cada Amaní, Bella Vista - Delgaditas-Guarinó. grupo y su área de uso. El esfuerzo de muestreo acumulado Para estimar la densidad poblacional de S. leucopus en es- en el DMI Charca de Guarinocito fue de 64 horas/hombre. tas localidades se hizo uso del método de muestreo por distancias con transectos lineales (Buckland et al., 2001). El muestreo por distancia es uno de los métodos más efi- Este método implica contar los animales vistos por un ob- cientes para estimar densidades poblacionales. Es decir, uno servador que camina a lo largo de una línea de transecto, de los métodos que produce estimados válidos y más preci- midiendo la distancia perpendicular hasta el punto donde sos (i.e., con menor varianza muestreal) para un esfuerzo de se observó el animal o hasta el centro geográfico del grupo muestreo dado (Buckland et al., 2001; Harris y Burnham, observado (Buckland et al., 2010). El rumbo, la distancia y 2002; Norvell et al., 2003; Kissling y Garton, 2006; Somer- orientación de los transectos establecidos en cada localidad shoe et al., 2006). Por esta razón, se asume que los estimados dependió del tamaño, la topografía y la forma de bosque de densidad poblacional obtenidos con este método y con evaluado en cada una (Tabla 2). conteos completos son comparables (Yoccoz et al., 2001).
Tabla 2. Número de transectos y esfuerzo de muestreo por localidad.
Localidad Número Longitud media Esfuerzo total de transectos de transectos m (DE) de muestreo (km) RNSC Río Manso 35 263 (76) 108.45 La Habana 16 288 (75) 109.62 RNSC Venecia – Jagual 18 319(14) 100.44 Amani 38 622(304) 197.62 Carrizales 5 1,100 (12) 44.84 Los Mangos 5 860 (22) 28.5 Sasaima 4 720 (150) 41.9 Cañaveral 2 550 (50) 8.8 La Clara 5 750 (48) 35.92 Tras. Manso 17 550 (60) 37.66 Bella Vista – Guarinó – Delgaditas 52 300 (62) 428.38 Neotropical Primates 26(1), September 2020 59
Análisis de datos se hizo por medio de un gráfico de intervalos de confianza (IC). Cuando los IC de dos estimados de densidad presen- La densidad poblacional de Saguinus leucopus se estimó con taron un traslape mayor a un 25 %, se consideró que no el programa DISTANCE 7.0 (Thomas et al., 2009). El había evidencia de que las densidades poblacionales entre objetivo del análisis es ajustar una función de detección a ambos fueran significativamente diferentes, con un nivel de la distribución de frecuencias de las distancias perpendicu- confianza del 95 % (Cumming et al., 2007). lares de las observaciones (Thomas et al., 2002) utilizando seis modelos teóricos. El mejor modelo se seleccionó con Resultados base en el menor valor del criterio de información de Akai- ke (AIC), (Buckland et al., 2001). La varianza de la den- RNSC Rio Manso: Durante el muestreo se lograron 44 re- sidad (CV) para Río Manso fue estimada asumiendo que gistros visuales de S. leucopus. El modelo Uniforme con la distribución de la tasa de encuentro se ajustaba a la dis- serie de expansión Coseno arrojó el valor más bajo del tribución Poisson de probabilidad (Buckland et al., 2001); criterio de información de Akaike (AIC) y mejor ajuste en la Habana, Venecia y Amaní se hizo la estimación de la de las distribuciones observada y esperada de distancias varianza empíricamente. En todas las localidades se usó el perpendiculares. El tamaño de los grupos varió entre tamaño de grupo estimado tomado del análisis de regresión uno y seis individuos, estimando un valor medio de 4.23 entre el tamaño de grupo y la probabilidad de detección (IC95 % = 3.5 – 5). Se estimó una densidad poblacional de para el cálculo de la densidad. 55 individuos/ km2 (IC95 % = 35 − 85) y 13 grupos/km2 (IC95 % = 9 − 20), con un coeficiente de variación del 22.5 Comparación de las densidades poblacionales de S. leucopus y 20.6 % respectivamente. La varianza de la densidad estu- para las localidades en la que se hizo segunda replica temporal vo compuesta por la probabilidad de detección en un 39 %, La comparación entre las densidades estimadas para S. leu- por la tasa de encuentro en un 44.9 % y por el tamaño de copus entre la presente evaluación y las estimaciones hechas grupo en un 16.1 %. Los resultados de esta y las otras lo- en Amaní (Sanchez-Londoño, 2013, datos tomados en calidades están resumidos en las Tablas 3 a 6 y pueden ser 2006), Charca de Guarinocito, RNSC Río Manso, RNSC leídos siguiendo el anterior formato en el mismo orden en Venecia (Roncancio et al., 2011, datos tomados en 2008), el que están las tablas.
Tabla 3. Modelos ajustados basados en la distribución de las frecuencias de las distancias de detección de las observaciones de Saguinus leucopus para cada localidad.
Localidad Número Modelo Serie de registros de expansión
Charca de Guarinocito - - -
RNSC Río Manso 44 Uniforme Coseno
La Habana 39 Semi-normal Coseno
RNSC Venecia – Jagual 26 Semi-normal Coseno
Amani 59 Uniforme Coseno
Bella Vista – Guarinó – Delgaditas 45 Semi-normal -
Tabla 4. Tamaño de grupo de Saguinus leucopus para cada localidad.
Localidad Tamaño Tamaño grupo Rango de grupo IC 95 %
Charca de Guarinocito 5.3 - 5 - 6
RNSC Río Manso 4.23 3.5 - 5 1 - 6
La Habana 4.9 3.9 – 6.1 1 - 7
RNSC Venecia – Jagual 2.9 2.13 – 4.02 1 - 7
Amani 3.37 2.9 – 3.9 1 - 8
Bella Vista – Guarinó – Delgaditas 3.76 3.05 – 4.62 1 - 7 60 Neotropical Primates 26(1), September 2020
Tabla 5. Densidad poblacional de individuos de Saguinus leucopus para cada localidad. CV D=Coeficiente de variación de la densidad de individuos.
Localidad Densidad Densidad CV D Densidad poblacional Ind/km2 IC 95 % Grupos/km2 Charca de Guarinocito 75 - - 14.2 RNSC Río Manso 55 35 - 85 22.5 13 La Habana 109 63 - 191 25.6 22 RNSC Venecia 40 20 - 77 30.6 13 Amani 47 29 - 78 25 11 Bella Vista – Guarinó –Delgaditas 14 8.4 – 21.9 25 3.6
Tabla 6. Componentes de la varianza de la densidad poblacional de Saguinus leucopus para cada localidad.
Componentes de la varianza Charca de RNSC Río La RNSC Amaní Bella Vista – Guarinó de la densidad Guarinocito Manso Habana Venecia -Delgaditas Probabilidad de detección - 39 37.6 49.3 14.1 28 Tasa de encuentro - 44.9 45 30.5 74.1 54.2 Tamaño de grupo - 16.1 17.4 20.2 11.8 17.8
Comparación de la densidad de Saguinus leucopus para las Por otro lado, para Amaní no se encontró un cambio sig- localidades en la que se hizo segunda replica temporal nificativo en la densidad poblacional de S. leucopus con Para la Charca de Guarinocito se registró un aumento de dos respecto a los resultados de 2006 (Sanchez-Londoño, individuos en la abundancia total pero mantiene el número 2013) (Fig. 2). No obstante, es necesario tener en cuenta de grupos. En este sentido, la “población” en este DMI es que el muestreo en el 2006 se hizo sobre un área inferen- consistente con el muestreo llevado a cabo en 2008 (Roncan- cial de aproximadamente 5.5 km2, los cuales representan cio et al., 2011) (Fig. 2). En la RNSC Río Manso los resul- poco más del 20 % del presente esfuerzo y que estuvo fo- tados reflejan una disminución significativa en la densidad calizada en el sector de Los Mangos con un tamaño mues- poblacional del primate de un 61 %. Asumiendo un modelo treal de solo cinco transectos. En Amaní, se encontraron lineal en la tasa de crecimiento poblacional podría estimarse diferencias numéricas entre algunos de los seis sectores una reducción anual continua de alrededor del 8.7 %. Igual- evaluados. Si bien, dada la cantidad de datos que se ob- mente, para la RNSC Venecia – Jagual se encontró una dis- tuvieron por sector no es razonable hacer un análisis por minución significativa de un 70 % en el parámetro para una bloques de la densidad, es plausible, asumiendo que la disminución lineal anual estimada del 9.8 % (Fig. 2). probabilidad de detección de la especie entre los secto- res es igual (mismos observadores, coberturas vegetales similares, muestreo hecho en un corto periodo de tiempo, condiciones ambientales constantes y homogéneas), que la comparación se puede hacer a partir de las abundancias relativas (número de registros por kilómetro recorrido). En este sentido se detectó que los sectores de la Clara y Carrizales presentaron las abundancias relativas más ba- jas, siendo numéricamente entre 3 y 25 veces menores que en las otras localidades.
Tabla 7. Abundancias relativas (número de registros por kilóme- tro recorrido) de grupos e individuos de tití gris (Saguinus leuco- pus) en los diferentes sitios evaluados en el área de influencia del embalse Amaní.
Figura 2. Análisis gráfico comparativo de las densidades del pre- Sitio Grupos/km Individuos/km sente muestreo con estimaciones previas para el DMI Charca de Guarinocito, RNSC Río Manso, RNSC Venecia (Roncancio, Berlín 0.35 1.25 2011) y Amaní (Sanchez-Londoño, 2013). Cuando los IC de dos estimados de densidad presentan un traslape mayor a un 25 %, se Cañaveral 1.48 3.86 considera que no hay evidencia de que las densidades poblacio- Carrizales 0.18 0.54 nales en ambos son significativamente diferentes,con un nivel de confianza del 95 % (Cumming et al., 2007). Neotropical Primates 26(1), September 2020 61
Sitio Grupos/km Individuos/km inmaduros lo que sugiere el sacrificio del parental en la captura y baja probabilidad de soportar las condiciones de Clara 0.06 0.17 cautiverio (Duarte-Quiroga y Estrada, 2003). Mangos 0.74 2.18 Sasaima 0.26 0.88 Basados en la información informal de las comunidades locales, el tráfico de fauna en la zona puede estar asociado al aumento de la accesibilidad de foráneos después de la Discusión desmovilización en el 2006 de los grupos de paramilita- res y al progresivo desmantelamiento del frente 47 de las En este muestreo las densidades encontradas en el oriente de FARC consolidado en 2008. En algunos casos, los con- Caldas estuvieron entre 14 y 109 ind/km2. En contraste, en flictos socio políticos y la guerra pueden liberar la presión los muestreos llevados a cabo entre 2005 y 2008 las densi- sobre la biodiversidad productos de los cambios en los dades encontradas estuvieron entre 54 y 149 ind/km2 (Ron- patrones de asentamiento humano, la creación de zonas cancio et al., 2011). Puntualmente, dos de las cuatro áreas de protección de hecho y la reducción de las actividades en donde se hizo un segundo muestreo, RNSC Río Manso económicas basada en recursos (Hanson et al., 2009). y RNSC Venecia – Jagual presentaron reducciones del 61 y Adicionalmente, en muchos escenarios, los traficantes 70 % respectivamente con respecto al 2008. Esta reducción pueden desconocer o pueden no sentirse afectados por fue apenas detectable por la magnitud del cambio. Tener la la legislación o el costo para ellos por apegarse a la ley capacidad de detectar cambios menores implica incrementar llega a ser más grande que no hacerlo y las penas pueden el tamaño de la muestra (Field et al., 2005). En ese sentido ser menores que la ganancia por el tráfico (Dutton et al., es necesario gestionar los recursos suficientes para hacer los 2013). Este antecedente determina la necesidad del for- muestreos completos y alcanzar la precisión requerida para talecimiento institucional que incluye la articulación de concluir que efectivamente no hubo cambios, prinicipal- las diferentes instancias de control (autoridad ambiental, mente reducciones y no que simplemente no fueron detec- fuerzas policivas y militares, jueces y fiscales) para la ges- tados, es decir, mejorar la potencia estadística y reducir la tión efectiva de las áreas protegidas y en general de los re- probabilidad de cometer un error tipo II en el rechazo de la cursos naturales en los escenarios actuales de post-acuerdo hipótesis (Lindermayer y Likens, 2009; Mcdonald-Madden y posconflicto. En ese sentido, el control efectivo im- et al., 2010; Reynolds et al., 2011). plica un abordaje multifocal que incluye la educación y comunicación hacia las comunidades buscando reducir la A pesar de las 20,000 ha que se han perdido en el oriente tolerancia a estas prácticas en su territorio, modificando la de Caldas en los últimos 10 años, la RNSC Río Manso y actitud de las personas hacia la especie, el contexto social Venecia el Jagual no han sido afectadas. La reducción de la y posicionando la norma; revisando la dependencia eco- densidad de S. leucopus en estas dos localidades se puede nómica de las comunidades a estas actividades, generando atribuir al tráfico, tal y como lo confirmó el propietario de la conversión de los sistemas productivos y fortaleciendo Venecia - el Jagual quien declaró que en el 2013 se presen- la capacidad de gestión interinstitucional e intersectorial taron ingresos de traficantes a la reserva y que extrajeron para planear e implementar con idoneidad técnica y ope- una gran cantidad de individuos del primate. En el caso de rativa las actividades de control y vigilancia (Warchol et Amaní, a pesar de no detectarse una reducción, la extrac- al., 2003; Shepherd, 2010; Daut et al., 2015). ción de Saguinus leucopus no se puede descartar, dado que la menor abundancia relativa en el sector bordeado por la Agradecimientos carretera entre Dorada y Norcasia (Sector La Clara), que no difiereaparentemente en otras condiciones de los otros Este trabajo fue llevado a cabo con recursos de compen- sectores, puede estar reflejando un impacto derivado de la sación obligatoria de Isagen. Agradecemos a Ana María mayor accesibilidad de potenciales traficantes (Laurance et Jaramillo de Río Manso y a Gustavo Toro de Venecia por al., 2008). permitirnos nuevamente el acceso a sus reservas, además de prestar el apoyo logístico para llevar a cabo los muestreos. 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corridor of protected areas and indigenous reserves of ca. Short Articles 10 million hectares in northwestern Amazonia, protects the Yuri, a group of isolated indigenous people, in order to guarantee their decision to not have contact with the ma- PRIMATE DENSITIES AT RÍO PURÉ NATIONAL joritarian society. The entire area of the park corresponds PARK, EASTERN COLOMBIAN AMAZONIA to a mainly flat surface, with some strongly undulating ar- eas, but without significant altitude differences, all over an Erwin Palacios area of ancient alluvial terraces; ninety-eight percent of the park´s area is covered with dense high terra firme forest, Introduction while flooded forest comprises just 1.0 % of the area and is concentrated along the Puré River and its main tributar- Colombia is one of the three most megadiverse countries of ies (Quebrada Aguanegra, Quebrada Arapa, Caño Mateo) the world (Mittermeier et al., 1997; Butler, 2019). Among and the various systems of lakes dispersed along the river´s primate diverse countries, Colombia is fifth, after Brazil, course; the remaining area corresponds to a mix of nine Madagascar, Indonesia and the Democratic Republic of additional types of forests (IGAC, 1999; Instituto Sinchi Congo (Mittermeier, 2013) with 38 primate species and 45 et al., 2000; Murcia et al., 2014). According to the Na- taxa (APC, 2005). Protected areas in Colombian Amazonia tional Parks Unit (2015), based on studies of the Sinchi represent a significant proportion of the known distribu- Institute, 1,583 species of vascular plants belonging to 133 tion area in the country of some primate species (Lagothrix families have been recorded in the park, among which the lagothricha, L. lugens, Ateles belzebuth, Cacajao melanoceph- best represented are Rubiaceae, Annonaceae, Moraceae, alus, and Pithecia hirsuta amongst others). Nevertheless, Mimosaceae, Fabaceae and Sapotaceae; 252 bird species, there is still scarce knowledge about their population sta- belonging to 46 families were recorded for the park in four tus within such protected areas, as historically few research different sites (Alarcón-Nieto, 2007). activities have been conducted either by primatologists or other researchers, due to the presence of illegal armed groups over decades, and the difficulty and logistical costs to reach very isolated regions. There are also populationsof these species outside of protected areas, but in many cases, they are subject to diverse sources of anthropogenic distur- bance, and information on their status is also very limited.
This gap of information does not allow us to put into per- spective (qualify and quantify) the role of protected areas in conserving primate fauna and weakens government and nongovernment institutions´ strategies for protected are- as and areas outside them, to effectively conserveprimates and wildlife in general; it also limits the ability to make informed decisions when working with local communities to implement participative conservation strategies in their territories.
As part of an effort of Conservation International Colom- bia to generate data on the abundance of about 24 medium and large vertebrate species in eastern Colombian Amazo- Figure 1. Interfluvial region between the Caquetá and Putumayo nia, including within protected areas and indigenous re- Rivers in Colombian Amazonia, where survey sites inside the Río serves, a series of standardized line-transect surveys were Puré National Park are indicated. carried out in four forest sites within Río Puré National Park (hereafter Río Puré NP) to document the densities Methods of primate species in one of the most isolated regions of Colombian Amazonia. Linear transects Between 2000 and 2006 I carried out surveys in four sites Study site in Río Puré NP: Quebradón El Ayo (1°35’S, 69°30’W), Caño Mateo (2°08´S, 69°49´W), Caño Esperanza (1°50’S, The Río Puré NP is located in the interfluvial area between 69°43’W) and Quebrada Arapa (2°19´S, 69°44´W) (Fig. 1). Caquetá and Putumayo rivers in the Amazonas depart- All of these sites except Q. El Ayo are located in the core area ment, southeastern Colombia (Fig. 1). The park, declared of the park, between 42 and 70 km away from the closest in 2002, comprises 999,880 ha of primary forest, and along human settlement, including those of the Yuri people, more with conserving biological diversity and complementing a than 80 km away. Access to these sites is only possible by Neotropical Primates 26(1), September 2020 65 river, after navigating the Caquetá/Japurá River to reach the density estimates, using ungrouped perpendicular distances mouth of the Purué River (Puré in Colombia) and then nav- from transect to the first animal sighted. Animals detected igating it further within Brazilian lands to reach the border by acoustic signals but not sighted within the transect area between Brazil and Colombia; a boat trip of nearly 600 km, were not included in the analysis. Whenever necessary, I plus 12-120 km after leaving the Puré River and navigating truncated five percent ofthe outlying data, and pooled data towards the headwaters of its first and second order tribu- across different sites forthose species with a small number taries, selected in advance to establish the survey transects. of detection events, in order to strengthen the site-specific Camps sites were always at least 3 km in a straight line from density estimates. For this subset of species with a limited the closest major water course (from Japurá River, 9.5 km sample size, density estimates (D) were calculated using: Q. El Ayo; from Puré River, 3.5 km C. Mateo and 24 km Q. Arapa, and, from Quebrada Agua Negra –the major tributary D = ND/L* 2(ESW) of Puré River, 10 km C. Esperanza), and high ground was always selected, given that water level in such small second where: order (12-15 m wide) tributaries varies significantly accord- D = Group density (groups per km2); ing to local rainfall, causing variations of up to 2 meters in ND= Number of sightings for each species; the water level from one day to another. At each site (except L = Cumulative transect length walked in each site; in the Ayo, where just two were cut), three 5-km linear tran- ESW = Effective strip width, defined as the largest per sects were cut and marked with colored flagging tape every pendicular distance observed for each species, but 50 meters to facilitate the accurate positioning of sightings, excluding obvious outliers. and they were left to rest at least for one day before starting censuses. Starting points of transects were positioned at least This was the case for the white-fronted capuchin (Cebus al- 300 m away from the camp sites. Sightings were recorded bifrons), the squirrel monkey (Saimiri cassiquiarensis), and in accordance with standardized and widely used method- the red howler (Alouatta seniculus), which were regularly ologies (Peres and Cunha, 2011). Each transect was walked recorded three or fewer times at a given site. For species by an independent observer during days without rain at a living in large, non-cohesive groups—such as the woolly continuous speed of 1.25 km/h, between 06:30-11:15 h and monkey (Lagothrix lagothricha) —which can spread out between 13:30-16:30 h; during return walks, average speed over hundreds of meters in the forest, I added one third increased slightly (1.6 km/h) but this did not affect detec- of the mean group spread to the ESW estimated by DIS- tion probabilities. Over the years, a group of 8 people from TANCE in order to avoid inflated-density estimates (Pe- local indigenous communities of the lower Caquetá River res, 1997). Mean group sizes, derived from reliable group (ca. 120 km north towards the Park) has been trained in line counts, were then multiplied by group density estimates transect methodology and participated in large vertebrate in order to obtain mean population densities at each site. surveys in eastern Colombian Amazonia, including those Crude population biomass was calculated using the mean at Río Puré NP. At each survey site a team of four people body weight of a given species, defined as 80 percent of was able to alternate walks on the different transects in order the average adult body weight of males and females of each to minimize estimation biases for perpendicular distances. species (Peres, 1993), multiplied by its density estimate. Every 3 days a different member of the team was able to rest. We expected to carry out a 300-km census at each site, but Results this was not possible due to adverse weather conditions; cen- sus effort totaled 989.7 km (200.7 km Q. El Ayo, 288 km C. The meanprimate population density for all sites was 64.4 Mateo, 251 km C. Esperanza and, 250 km Q. Arapa). individuals per square kilometer. The highest total pri- mate density was found at Quebradón El Ayo (86.9 ind/ Every time we detected any of the target species, we re- km2), while the lowest was at Caño Mateo (42.5 ind/ corded its location along the transect and the perpendicular km2). Both, Quebrada Arapa and Caño Esperanza had distance to the animal observed. We recorded the number similar intermediate total primate densities (Table 1). of individuals, and, to the extent possible, we attempted a Total aggregated biomass showed a somewhat similar pat- complete count of the group´s individuals, for which we tern, with the highest primate biomass at Quebradón El did not spend more than 15 minutes. Sightings made dur- Ayo (169.5 kg/km2) and Quebrada Arapa (157 kg/km2), ing return walks were also recorded and contributed to the and the lowest at Caño Mateo. Biomass at Caño Esperan- detection models, and allowed us to get a more accurate es- za reached an intermediate value (Table 1). Mean aggre- timate of the mean group sizes (see Palacios & Peres, 2005). gated biomass for the four surveyed sites was 133.9 kg per Group spread distance for large non-cohesive groups (e.g., square kilometer. Differences in density and total biomass woolly monkeys or squirrel monkeys) were also estimated. between sites were driven both by the large-bodied wool- ly monkeys, Lagothrix lagothricha, and the medium-sized Population density estimates brown capuchin, Sapajus apella. For example, woolly Data were analyzed with DISTANCE 5 software. Either monkey densities at C. Esperanza and Q. Arapa were be- the hazard rate or half-normal models with a cosine adjust- tween 1.5 and 2.0 times higher than in C. Mateo and Q. ment (Buckland et al., 1993) were used to obtain group Ayo and represented 47.2 and 60.9 percent of their total 66 Neotropical Primates 26(1), September 2020 primate biomass, while this species only represented 28.5 3.6 and 1.8 ind/km2 of C. albifrons – Palacios and Peres, percent and 36.0 percent of the total primate biomass at 2005) and at Quebradón El Ayo ( 30.4 ind/km2 of S. apella Q. El Ayo and C. Mateo respectively. On the other hand, vs. 2.5 ind/km2 of C. albifrons). Nevertheless, the oppo- S. apella density at Q. El Ayo represented a very particular site situation occurred in C. Mateo and C. Esperanza (6.5 case, as it was between 4.1 and 15.2 times higher than in and 4.6 ind/km2 of C. albifrons respectively, vs. 2.0 and any other site surveyed in this study. Consequently, its 3.4 ind/ km2 of S. apella), suggesting that such ecological biomass at Q. El Ayo represented 35 percent of the total displacement may operate in both ways, although ecologi- primate biomass. There were also remarkable differences cal factors directing it are still unknown. in the densities of Cebus albifrons, Saimiri cassiquiarensis and Leontocebus fuscus between the surveyed sites, espe- Total primate density at all but one of the four sites (Caño cially for L. fuscus (1.3 to 3.7 times higher at C. Esperanza Mateo) surveyed in Río Puré NP was higher than that and Q. Arapa), but these did not significantly affect the reported by Defler (2013) (47.9 ind/km2) for his site on total primate biomass at any particular site. Other species the right bank of the Puré River. C. Mateo is ca. 23 km such as Alouatta seniculus, Cheracebus lucifer and Pithecia away from Defler´s site, and both sites are relatively close hirsuta showed minor differences in their densities. Pri- to the Puré´s main course, therefore being more accessi- mate biomass represented between 36 percent and 49.1 ble to commercial hunters of spotted cats, that during the percent of the total large vertebrates aggregated biomass late 60´s and the 70´s intensively used large primates and at the surveyed sites (Palacios, unpublished data). During other medium and large-sized vertebrates as bait. Hunt- census walks we never recorded Cebuella pygmaea, but at ers´ parties periodically entered into the current Río Puré Caño Esperanza, on a rainy afternoon before starting cen- NP area and established camps along the Puré river and suses, at around 17:30h three individuals of the species its tributaries for long periods (2-3 months) during which got tangled in a mist net we inadvertently left unfolded they processed and accumulated the skins and then took after carrying out bird sampling. them to La Pedrera to the merchants who sponsored such raids (Elías Yucuna and Julián Yucuna, Pers. comm.). The Discussion primate density figures for these two sites are 25 %-51 % Population densities of mid-sized and small primates were lower than those for the three additional sites surveyed in similar to those estimated for other forests in western Am- Río Puré NP and might reflect the impact of hunting on azonia (Peres, 1990). In the majority of cases the densities the local primate populations. Defler (1980) reported that of Leontocebus fuscus, Saimiri cassiquiarensis, Cheracebus primate populations in the Mirití-Paraná River, Colombia, lucifer, and Pithecia hirsuta were in the range of densities affected by 20th century hide trade hunting had recov- previously reported for other sites in Amazonia. The re- ered, and Antunes et al. (2016) indicated that 70 % of all markable difference in Sapajus apella densities across sites populations of the lowest-fecundity and most prized game in the study suggests that particular ecological factors species affected by subsistence hunting (including Ateline could be determining the abundance of this species. For primates) currently occur at carrying capacity at both land- instance, the densities for the species at Caparú Biological scape and basin-wide scales. Station and Caño Pintadillo at the black-water lower Apa- poris River, and Q. El Ayo (20.4 – 30.9 ind/km2) (Palacios Nevertheless, it should be considered that in most recent and Peres, 2005) differ greatly from those at C. Mateo and times (during the decade of the 90´s, and through the first C. Esperanza (2 – 3.4 ind/km2), which in turn, are slightly five years of the 2000´s) dozens of dredges for gold mining higher to those estimated for the species at Curare indige- were permanently installed along the river and small trib- nous community (1.2 ind/km2) (E. Palacios, unpublished utaries, especially in the Brazilian portion (Purué River), data). Curare is an area subject to hunting pressure but, but also in the lower Puré at the Colombian side, entering can be considered as reflecting natural density ofS . apella, to the west farther than the C. Mateo, and also going up- as only five of 1,337 hunting events recorded in that com- stream the Quebrada Agua Negra; in addition, during late munity during ca. 10 years correspond to this species (E. 1990´s and early 2000´s a timber camp was established and Palacios, unpublished data). active very near to the Colombian-Brazilian border, near to Defler´s site. It is likely that the continuous need of pro- Defler (2003) has suggested that some type of ecological tein for dredge crews and loggers may have been fulfilled displacement between Sapajus apella and Cebus albifrons using the local wildlife populations, including large pri- could be the cause of the lower densities of the latter when mates such as Lagothrix. Density and primate biomass fig- both species are present in the same area. This suggestion ures for the species in all sites surveyed in this study except is partially supported by the density estimates of both spe- Caño Mateo lie in the range of the figures for the species cies at sites inside indigenous reserves north towards Río in 29 Amazonian non-hunted oligotrophic forests (Peres et Puré NP (Curare and Borikada, 1.2 and 8.8 ind/km2 of S. al., 2016). However, density of Lagothrix in Caño Mateo apella respectively, vs. 0 and 2.7 ind/km2 of C. albifrons – (4.5 ind/km2) was below the lower end (6.42 ind/ km2) of Palacios unpublished data), sites in the Yaigojé Apaporis the range of values calculated by Peres et al. (2016); pri- indigenous Reserve/National Park (Caparú and Caño Pin- mate biomass (36 %) was slightly higher than the lower tadillo, 30.9 and 20.4 ind/km2 of S. apella respectively, vs. end (28 %) at Caño Mateo, and right at the lower end at Neotropical Primates 26(1), September 2020 67 2 15 2.6 6.7 6.5 4.5 8.8 157 17.3 95.6 Kg/ km B 2 3.5 7.4 6.8 2.1 8.5 1.7 65.2 21.5 13.7 Ind/ km ID 0.7 3.7 1.3 2.5 2.3 2.3 0.32 0.75 2 13.87 Groups/ km GD 0.8 0.24 0.96 0.44 0.68 0.12 0.88 0.08 SR 6 3 2 24 11 17 22 20 N 105 5 5.8 5.7 2.7 6.7 3.7 10.5 20.2 MGS Quebrada Arapa (250 km) Quebrada p 2 2.8 8.2 4.4 9.1 11.2 18.8 48.8 Kg/ km B 103.3 p 2 61 3.7 4.8 4.6 4.2 6.6 26.5 10.7 Ind/ km ID p 0.7 0.6 0.4 0.6
4.67 1.91 3.26 2 12.14 Groups/ km GD p 0.4 0.6 0.3 0.2 1.2 1.23 1.03 SR 8 4 p 31 10 15 26 29 N 123 p 11 5.7 2.4 5.68 6.87 9.25 3.27 MGS Caño Esperanza (251 km) Caño 2 2.2 6.4 4.3 3.8 7.8 87.2 15.1 16.2 31.4 Kg/ km B 2 5 2 7.1 6.5 6.7 9.2 1.5 4.5 42.5 Ind/ km ID 2.8 0.3 1.52 1.16 0.69 2.94 0.44 0.67 2 10.52 Groups/ km GD 0.5 1.8 0.83 0.58 0.19 0.42 0.19 0.38 SR 7 7 18 30 21 15 65 14 N 147 4.7 5.6 2.4 6.7 7.3 3.4 6.7 3.14 MGS Caño Mateo (288 km) Mateo Caño 2 5.4 5.24 70.8 6.52 8.47 5.46 48.3 B Kg/ km sites in Río Puré National Park, eastern Colombian Amazonia. Park, National at four sites in Río Puré ) of primate species present 169.5 19.36 2 11 6.8 2.5 6.9 86.9 16.9 30.4 11.3 1.05 ID Ind/ km 2.8 14.3 3.02 4.24 2.63 0.25 0.63 0.21 0.54 2 GD Groups/ km and biomass (kg/km 2 0.9 ) 0.64 0.55 0.35 0.05 0.05 0.05 0,76 SR 7 1 1 1 74 16 11 18 19 N 4 5 10 18 5.6 7.2 2.6 12.7 MGS Quebradón El Ayo (200.7 km) Ayo El Quebradón Species Leontocebus fuscus Sapajus apella Sapajus Cheracebus lucifer Cheracebus Cebus albifrons Cebus Saimiri Saimiri cassiquiarensis Pithecia hirsuta Pithecia Alouatta seniculus Alouatta Lagothrix lagothricha MGS: Mean group size, N: Number of observations, SR: Sighting rate (number of sightings per 10 km of walked transect), GD: Group density, density, of observations,rate (number sightings per 10 km walked transect), GD: Group SR: Sighting N: Number size, group MGS: Mean during the censuses. at the site but not recorded p: species present B: Biomass, density, ID: Individual Density (individuals/km 2 1. Density Table
TOTALS 68 Neotropical Primates 26(1), September 2020
Quebradón El Ayo (28.5%). It is also well below the den- Josué Silva and, Gaudencio Silva (R.I.P.) for their hard work sity estimated for the species in the high Algodón River and camaraderie. Thanks also to Adriana Rodríguez for her (16.3 ind/km2) and just above the figure in the mid Tambo- incredible support, risking her life by being surrounded by ryacu River (3.5 ind/ km2), in the Napo-Putumayo Rivers a herd of wild peccaries while surveying large vertebrates in interfluvium in Perú, both sites highly affected by subsist- El Ayo, and Gustavo Alarcón, for his companionship and ence hunting and timber extraction (Aquino et al., 2016). bird skins´ specimen preservation sessions. Special thanks to Elías Yucuna ¨Machinchín¨, whose knowledge and mas- As previous surveys in eastern Colombian Amazonia have tership of the forest and Colombian Amazonian rivers has shown (Palacios & Peres, 2005; Defler,2013), low primate been fundamental over the years to reach those interesting densities and biomass at the forest sites surveyed at Río sites to survey. Thanks to the Colombian National Parks Puré NP seem to be a consequence of the limited habitat Unit for providing the research permit. primary productivity as a result of the very low fertility of soils in eastern Colombian Amazonia (IGAC, 1997, 1999; Erwin Palacios, Conservación Internacional Colombia, Defler, 2003). Soil data from samples collectedat Que- Carrera 13 # 71-41, Bogotá D.C., Estación Biológica Mo- bradón El Ayo, Caño Mateo and Caño Esperanza, every siro Itajura – Caparú, e-mail:
R. A., Rylands, A. B. and Wilson, D. E. (eds.) pp.13–26. of Rio de Janeiro, São Paulo and Paraná. The second spe- Lynx Edicions, Barcelona. cies is typically found in the phytoecological unit of Dense Mittermeier, R. A., Robles Gil, P. and Mittermeier, C. G. Rainforest, although there are also records of the species in 1997. Megadiversity, 501p., CEMEX, Mexico. Seasonal Semi-deciduous Forest and in Mixed Rainforest Murcia, U., Medina, R, Rodríguez, J. M., Castellanos, H., (Araucaria Forest), as well as in transition zones (Cunha et Hernández, A. and Herrera, E. 2014. Monitoreo de los al., 2009). The muriquis, like other large primates, tend to bosques y otras coberturas de la Amazonia Colombiana, occupy the higher strata of the forest (Peres, 1994). a escala 1:100.000. Datos del periodo 2012. Instituto Amazónico de Investigaciones Científicas Sinchi. Bogotá, According to information on the distribution of muriqui in D. C., 190 p., 2 Anexos. the state of Paraná, its occurrence extends to the north of Palacios, E. and Peres, C. A. 2005. Primate population the state in the municipality of Castro (Cunha et al., 2009). densities at three nutrient-poor Amazonian Terra Firme However, the distribution is restricted and poorly known, forests of Southeastern Colombia. Folia Primatol. 76(3): with records in 1994 that mention its occurrence in the mu- 135–145. nicipalities of Jaguariaíva and Guaraqueçaba (Martuscelli et Parques Nacionales Naturales de Colombia. 2015. Plan de al., 1994). Almost a decade later, a more southern popula- manejo reformulado del Parque Nacional Natural Río tion was registered by Koehler and collaborators (2002) in Puré. Accessed 10 October 2019. an isolated and unprotected fragment in the municipality Peres, C. A. 2008. Soil fertility and arboreal mammal bi- of Castro. The third confirmed record for Brachyteles arach- omass in tropical forests. In: Tropical Forest Community noides was in Olho D’Água farm, municipality of Doutor Ecology. Schnitzer, S. and Carson, S. (eds.) pp. 349–364. Ulysses (Ingberman et al., 2016). Apart from these few oc- Blackwell Scientific, Oxford, UK. currence records, the distribution and southern limit of this Peres, C. A., and Palacios, E. 2007. Basin-wide effects of species is little known, a concern for its conservation; the game harvest on vertebrate population densities in Am- species is classified as “critically endangered” in Paraná state azonian forests: implications for animal-mediated seed (Paraná, 2010) and as “endangered” nationally (ICMBio, dispersal. Biotropica 39: 304–315. 2018) and internationally (IUCN, 2019). Peres, C. A. and Cunha, A. 2011. Line-transect censuses of large-bodied tropical forest vertebrates: a handbook. Information related to the distribution and occurrence of Wildlife Conservation Society, Brazil. populations of the southern muriqui is fundamental for the Peres, C. A., Thaise, E., Schietti, J., S. J. M. Desmoulière proposal of conservation measures. Here we contribute new and T. Levi. 2016. Dispersal limitation induces long- occurrence records of the southern muriqui for Paraná state. term biomass collapse in overhunted Amazonian forests. PNAS 113(4): 892–897. Methods
We registered the occurrence of Brachyteles arachnoides NEW RECORDS OF BRACHYTELES ARACH- during mammalian fauna monitoring in two areas (Fig. 1). NOIDES (É. GEOFFROY, 1806) (PRIMATES: ATEL- The first area is a High Conservation Value area located IDAE) IN THE SOUTHERN ATLANTIC FOREST, at Taquarussu Farm, with 1,367 ha of preserved forest IN PARANÁ STATE, BRAZIL (24°47’44.2” S, 48°47’53” W) in the municipality of Adri- anópolis, PR, in the Vale do Ribeira region. The second Cláudia Golec Fialek area is a Private Reserve, the Reserva Particular do Pat- Mayara Cristina Gaspari rimônio Natural (RPPN) Vale do Corisco (24°12’16” S, Tiago Luiz Daros 49°21’26” W), with 396.6 ha, located at the eastern border Maria Harumi Yoshioka of the Environmental Protection Area (APA) of the Devo- Sérgio Bazilio nian Scarp, in the municipality of Sengés, PR. Both areas belong to the company Arauco Forest Brasil. Introduction Mammalian fauna were monitored in these areas between Primates of the genus Brachyteles Spix, 1923, popularly January 2015 and December 2019, for a total of 48 months known as muriquis or monos (Auricchio, 1995), are endem- of sampling, with an average of three days per month spent ic to the Atlantic Forest (Graipel, 2017). Thisbiome is com- in monitoring. Censuses were based in the analysis of di- posed in large part of extremely fragmented and reduced ar- rect (visualization and acoustic signals) and indirect meth- eas (Ribeiro et al., 2009), and is considered one of the most ods (analyses of footprints, marks and carcasses), together threatened biomes in the world (Myers et al., 2000). Two with camera traps. Species identification was made accord- species of muriqui are acknowledged to occur in different ing to specialized field guides (Becker and Dalponte, 2013; forest physiognomies: the northern muriqui, Brachyteles hy- Reis et al., 2009, 2014). poxanthus (Kuhl, 1820) in the states Minas Gerais, Espírito Santo, Rio de Janeiro and Bahia, and the southern muri- Monitoring was always performed by at least two ob- qui, Brachyteles arachnoides (É. Geoffroy, 1806) in the states servers in non-linear transects in search for traces of the 70 Neotropical Primates 26(1), September 2020 species. Transects included abandoned roads, natural 680 hours (340 hours per area), covering approximately trails and margins of streams, lakes and rivers. At the 965 km on foot or on motorized vehicle. end of the study period, we had actively searched for
Figure 1. Triangles - location of the records of B. arachnoides at Taquarussu Farm, municipality of Adrianópo- lis, and at the Reserva Particular do Patrimônio Natural Vale do Corisco, municipality of Sengés, PR. Circles represent occurrence records based on information in the literature and historical geographic range of B. arachnoides (gray area), adapted from species distribution modeling by Ingberman et al. (2016).
Figure 2. Photographs of the Brachyteles arachnoides female in the RPPN Corisco Valley. A = female resting; B and C = female moving through the forest canopy; D = the prehensile tail. Neotropical Primates 26(1), September 2020 71
Results Our records add new information about the distribution of Brachyteles arachnoides, principally for the state of Paraná. Here we present two new records of Brachyteles arachnoides In particular, we would like to highlight the importance for the state of Paraná. The first recordwas in the Vale of remaining forest areas along the Devonian Scarp. Al- do Ribeira, in the Taquarussu Farm, municipality of Adri- though many of these areas are fragmented and/or reduced, anópolis, in December 28, 2016, when a group of muriquis they can still support populations of various species. We was registered by their vocalizations. Due to difficulties in recommend surveys to evaluate the size of the population accessing points closer to the group, the individuals were of B. arachnoides in the area. This information could be not observed visually. The second record was on Novem- used to propose measures for the conservation and protec- ber 22, 2019, in the RPPN Vale do Corisco, municipality tion of the muriqui, especially in the Paraná State, where of Sengés, Paraná. On this day, a lone female was photo- information on the species is scarce. graphed and filmed in the forest canopy (Fig. 2). Cláudia Golec Fialek, Mayara Cristina Gaspari, Com- Discussion pany EKOS – Monitoramento da Fauna e Soluções Am- bientais - Rua Angelo Marcello, n° 200, Francisco Beltrão, Muriqui distribution in Paraná state is poorly known and PR., Tiago Luiz Daros, Maria Harumi Yoshioka, Arauco previously described populations are restricted to small do Brasil S.A. Avenida Iguaçu, 2820, Água Verde, Curiti- isolated forest fragments (Ingberman et al., 2016). Both ba, PR. And Sérgio Bazilio, University Estadual do Paraná the lack of knowledge and the isolation of populations (UNESPAR), Coronel Amazonas, União da Vitória, PR. are threats to the persistence of the species in the medium and long term. In addition, hunting and forest fires are References imminent threats to the preservation of muriqui in the state. Auricchio, P. 1995. Primatas do Brasil. Terra Brasilis, São Paulo, Brasil. Muriquis are relatively cautious and quiet, and they spend Cunha, A. A., Grelle, C. E. V., and Boubli, J. P. 2009. half of the diurnal hours at rest, so they may often go un- Distribution, population size and conservation of the noticed. When active they can move quickly through the endemic muriquis (Brachyteles spp.) of the Brazilian forest due to morphological adaptations such as the pre- Atlantic Forest. Oryx 43(2): 254–257. DOI: 10.1017/ hensile tail, long arms and hooked hands (Rosenberger and S003060530700230X. Strier, 1989). In addition, vocalization episodes of south- Graipel M. E., Cherem, J. J., Monteiro-Filho, E. L. A., and ern muriqui are less frequent than in the northern muriqui Carmignotto, A. P. 2017. Mamíferos da Mata Atlântica. (Talebi, 2005). In the two places that we registered the Pp. 391-482, In: Revisões em Zoologia: Mata Atlântica, muriquis, the species can be considered to be rare, because Monteiro-Filho E.L.A, Conte C.E. (Eds.), Ed. UFPR, despite all of our sampling efforts, the species was registered Curitiba. only once at each site. IUCN, 2019. The IUCN Red List of Threatened Species. Version 2019-2. Accessed 23 July 2019. Muriqui usually move around in groups that vary in com- ICMBio. 2018. Instituto Chico Mendes de Conservação position according to the season and food availability in da Biodiversidade. Livro Vermelho da Fauna Brasileira their natural habitat (Talebi and Lee, 2010). Sex-biased Ameaçada de Extinção. Brasília. Website: http://www. dispersal has been described for Brachyteles arachnoides, in icmbio.gov.br/portal/images/stories/comunicacao/publi- which adolescent females typically disperse from their na- cacoes/publicacoes-diversas/livro_vermelho_2018_vol1. tal group (Printes and Strier, 1999). The female registered pdf. Acessado em 28 de novembro de 2019. alone in the RPPN Vale do Corisco may have been forag- Ingberman, B., Kaminski, N., Fusco-Costa, R., and Mon- ing alone or perhaps emigrating. teiro-Filho, E. L. A. 2016. A new population of the endangered Brachyteles arachnoides (É. Geoffroy, 1806) Only three previous records are available for the muriqui in (Primates: Atelidae) in the state of Paraná, southern the state of Paraná. The record by Martuscelli et al. (1994), Brazil. Check List 12(3): 1906. DOI: http://dx.doi. in Jaguariaíva municipality (at the border with Sengés), in org/10.15560/12.3.1906. the Environmental Protection Area (APA) of Guaraqueça- Koehler, A. B., Pereira, L. C. M., and Nícola, P. A. 2002. ba remains unverified due to the lack of material proof New locality for the woolly spider monkey, Brachyteles (Ingberman et al., 2016). Koehler et al. (2002) reported arachnoides (E. Geoffroy, 1806) in Paraná state and the the occurrence of the species in Fazenda João Paulo II, urgency of strategies for conservation. Estudos de Biologia in the municipality of Castro, Paraná, in a small patch of 24 (49): 25–28. mixed forest along the rivers Ribeira and Açungui (Koe- Myers, N., Mittermeier, R. A., Mittermeier, C. G., Fon- hler et al., 2002). Another population was registered in seca, G. A. B., and Kent. J. 2000. Biodiversity hotspots the Olho D’Água Farm, municipality of Doutor Ulysses for conservation priorities. Nature 403: 853–858. DOI: (Ingberman et al., 2016). 10.1038/35002501 72 Neotropical Primates 26(1), September 2020
Martuscelli, P., Petroni, M., and Olmos, F. 1994. Fourteen new localities for the muriqui (Brachyteles arachnoides). PITHECIA MITTERMEIERI (MARSH, 2014) Neotrop. Primates 2(2): 12–15. GEOGRAPHIC DISTRIBUTION: NEW RECORDS Paraná. Publicado no Diário Oficial n° 8233, de 1 de jun- EXTEND THE RANGE EAST OF THE JURUENA ho de 2010. Reconhece e atualiza Lista de Espécies de RIVER Mamíferos pertencentes à Fauna Silvestre Ameaçadas de Extinção no Estado do Paraná e dá outras providências, Almério Câmara Gusmão atendendo o Decreto N° 3.148 de 2004, 2010. Odair Diogo da Silva Pereira, M. C. B. and Scroccaro, J.L. 2010. Bacias Hi- Ana Lúcia Cardoso Martins drográficas do Paraná. Série histórica. Curitiba: SEMA. Vancleber Divino Silva Alves pp.138. Manoel dos Santos Filho Pereira, A. D., Bazilio, S., Yoshioka, M. H. 2018. Mamíferos de médio e grande porte em fragmentos de Introduction Floresta Ombrófila Mista, Sul do Brasil. Boletim da Socie- dade Brasileira de Mastozoologia, 83: 119–125. The range of Mittermeier’s saki monkey (Pithecia mitter- Peres, C. A. 1994. Which are the largest New World mon- meieri) (Primates: Platirrhini) was originally proposed to keys? J. Human Evol. 26: 245–249. extend throughout the region east of the Madeira River up Printes, R. C., and Strier, K. B. 1999. Behavioral correlates to the Juruena River as well as along the entire Guaporé of dispersal in female muriqui (Brachyteles arachnoides). River (Marsh, 2014). It had been suggested by Miran- Int. J. Primatol. 20: 941–960. da-Ribeiro (1914), Hershkovitz (1987) and Sampaio et al. Reis, N. R., Fragonezi, M. N., Peracchi, A., Shibatta, O. (2012) that the taxon that corresponds to the modern P. A., Sartore, E. R., Rossaneis, B. K., Santos, V. R., and mittermeieri also exists east of the Juruena River. How- Ferracioli, P. 2014. Mamíferos terrestres de médio e grande ever, this distribution was not followed by Marsh (2014), porte da Mata Atlântica: guia de campo. Technical Books, who instead restricted its distribution to the region west of Rio de Janeiro. this river. The name Pithecia mittermeieri is deployed here, Reis N. R.; Peracchi, A. L., Fragonezi, M. N., Rossaneis, despite questions about the validity of the Pithecia taxon- B. K. 2009. Guia ilustrado mamíferos do Paraná, Brasil. omy of Marsh (2014) raised by Serrano-Vilavicencio et al. Editora USEB, Pelotas, RS. (2019). Genetic studies are needed to resolve the relation- Reis, N. R., Peracchi, A.L., Pedro, W.A., Lima, I. P. 2011. ship between P. mittermeieri and P. irrorata. Mamíferos do Brasil. 2ª ed. Nélio R. dos Reis. Londrina. Ribeiro, M. C., Metzger, J. P., Martensen, A. C., Ponzo- Recently, new populations of Pithecia mittermeieri have ni, F. J., Hirota, M. M. 2009. The Brazilian Atlantic been recorded in the Upper Paraguai River Basin (De La- Forest: How much is left, and how is the remaining zari et al., 2014; Gusmão and Santos-Filho, 2015; Orsini forest distributed? Implications for conservation. Biol. et al., 2017). Some of these records (24 and 26, Fig. 1) not Conserv.142:1141–1153. only extend the range of P. mittermeieri 300 km south-east- Rosenberger, A. L., and Strier, K. B. 1989. Adaptive radia- ward, but they are also the easternmost points for the genus tion of the Atelinae primates. J. Hum. Evol. 18: 717–750. as a whole in Mato Grosso state, Brazil. They also represent Talebi, M. 2005. Factors affecting food choices and di- new population records in the ecotonal region between the gestive efficiency of the critically endangered muriquis Amazon, Pantanal, and Cerrado. Such new sites suggest- (Brachyteles arachnoides - Primates- E. Geoffroy, 1806) ed that P. mittermeieri species distribution was greater than of Brazilian Atlantic Forest. Doctoral thesis. Biological that formerly recognized, and here we report additional re- Anthropology, University of Cambridge, Cambridge, UK. cords that extend the species’ geographical distribution still Talebi, M. and Lee, P. 2010. Activity patterns of southern farther eastward. muriqui (Brachyteles arachnoides - Atelidae) in the largest remaining fragment of Brazilian Atlantic Forest. Int. J. Methods and observations Primatol. 31: 571–-583. Our survey was conducted at Fazenda Camargo Correa in the municipality of Diamantino, state of Mato Grosso, in a 307,880 ha block of continuous terra firma forest. Cer- radão enclaves (RadamBrasil, 1978) are also present. The area is located on the Chapada dos Parecis (Fig. 1, point 28). The climate of the region is AW with 1,900mm mean annual rainfall, and 23°C mean annual temperature (Alva- res et al., 2014).
Primate surveys were conducted using line-transect meth- odology adapted from Peres (1999), where three trails were Neotropical Primates 26(1), September 2020 73 traversed every morning (from 5h to 12h) from October five individuals, including one juvenile and four adults 5th to October 15th, 2018, with a total of 106 km of sam- and subadults in the second. Subsequently, locality records pling effort. All vegetation strata were scanned to locate available in Sampaio et al. (2012), Marsh (2014), Gusmão and identify members of the regional primate fauna. Dur- and Santos-Filho (2015) and Orsini et al. (2017) were ing the survey period, two Pithecia mittermeieri sightings compiled along with those from the current study in order were obtained (Fig. 2) while groups of the animals were to produce a map with all known records for the species moving along tree branches. Seven adults and subadult (Fig. 1). The corresponding updated species occurrence individuals were observed during the first sighting,and records are provided in Table 1.
Figure 1. Distribution map of Pithecia mittermeieri, with squares indicating the locations available in the literature, and the star the new locality from this study. Numbers correspond to locations listed in Table 1.
Figure 2. Adult male Pithecia mittermeieri photographed in Fazenda Camargo Correa, Diamantino munic- ipality, Mato Grosso state, Brazil. Photo: O. D. S. 74 Neotropical Primates 26(1), September 2020
Table 1. Records of Pithecia mittermeieri obtained from the literature and from field data in Brazil.
Area Locality Latitude (S) Longitude (W) Reference
1 Amorin, Brabo, Limoatuba (Olalla collection, by 02°25’16” 055°07’30” Marsh (2014) gazetteer, Paynter Jr. & Traylor Jr. 1991) 2 Rio Arapiuns, Aruá (Olalla collection, by gazetteer, 02°39 055°37’59” Marsh (2014) Paynter Jr. & Traylor Jr. 1991 3 Limoal near Boim (Olalla collection, by gazetteer, 02°43’ 05” 055°13’23” Marsh (2014) Paynter Jr. & Traylor Jr. 1991) 4 Parintins, Amazonas 02°37’12” 056°52’48” Marsh (2014) 5 Rio Andira 02°46’12” 057°03’36” Marsh (2014) 6 Lago Andira 02°45’ 057°09’36” Marsh (2014) 7 Itaituba, Villa Braga 04°25’00” 056°16’59” Marsh (2014) 8 Igarapé Auara (Olalla collection, by gazetteer, Paynter 04°17’13” 059°25’48” Marsh (2014) Jr. & Traylor Jr.1991) 9 Borba 04°24’00” 059°34’59” Marsh (2014) 10 Rio Aripuanã 05°11’38” 060°23’35” Marsh (2014) 11 Lago do Cipotuba 05°32’06” 060°22’23” Marsh (2014) 12 Humaitá, Amazonas 07°25’44” 063°00’07” Marsh (2014) 13 Destacamento do Ribeirao (Natterer 1883) 10°15’ 065°16’ Marsh (2014) 14 Rio Pacáas Novos (Natterer 1829) 10°48’07” 065°07’41” Marsh (2014) 15 Nova Brasília (PoloNoreste 1985) 10°44’24” 10°44’24” Marsh (2014) 16 Cacoal State Park 11°09’ 061°34’ Marsh (2014) 17 Chupinguaia 12° 061° Marsh (2014) 18 Retiro do Veado Branco, Serra do Norte (Comissão 11°19’59” 059° Marsh (2014) Rondon) 19 Km 16 on BR 230 (approx.) 07°32’17” 062°44’53” Marsh (2014) 20 Cravari, Mato Grosso 14°49’ 60° 6’ Hershkovitz (1987) 21 Tapirapuã, Rio Cipotuba, Mato Grosso 12°56’ 58°40’ Hershkovitz (1987) 22 Brasnorte, Mato Grosso 12°32’ 57°52’ Sampaio et al. (2012) 23 Pontes & Lacerda, Mato Grosso 15°01’ 59°37’ Sampaio et al. (2012) 24 Tangara da Serra, Mato Grosso 14°35’23” 057°24’27” Gusmão and Santos-Filho (2015) 25 RPPN Água Boa, Cacoal, Rondônia 11°29’ 061°26’ Gusmão et al. (2014) 26 Lambari do Oeste, Mato Grosso 15°11’42” 057°44’43” Orsini et al. (2017) 27 Linha 9, km 3.5, Cacoal, Rondônia 11°28’ 61°21’ Cavalcante et al. (2018) 28 Fazenda Camargo Correa, Diamantino, Mato Grosso 14°16’9” 56°40’13” Current study
Discussion corresponding to an extension of more than 90 km within the Chapada dos Parecis. As the species had been reported The data presented in this study reinforce the opinion only within the Amazon until now, and the current study voiced in Sampaio et al. (2012) that geographical distri- took place in the extreme southeastern edge of the Amazon bution extensions were likely for this species in the eastern rainforest, Pithecia mittermeieri seems unlikely to be found Juruena River region. Gusmão and Santos-Filho (2015) beyond these limits. extended the range some 200 km to the east, and Orsini et al. (2017) recorded another population about 70 km to Acknowledgments the south of the limit proposed of Gusmão and Santos-Fil- ho (2015). The eastern-most known records available in We thank Coordenação de Aperfeiçoamento de Pessoal de Mato Grosso state are those given in this study, an eastern Nível Superior (CAPES) for a Ph.D. scholarship to A.C.G. extension for the genus range as a whole in Mato Grosso, and Msc. scholarships to O. D. S. and A. P. D. B. We also Neotropical Primates 26(1), September 2020 75 thank the Fundação de Amparo à Pesquisa do Estado de Miranda Ribeiro, A. 1914. Historia Natural Zoologia. Mato Grosso (FAPEMAT) for V. D. S. A. Msc scholarship Mamíferos. Comissão de Linhas Telegráficas Estratégicas de and for research financing (Edital n° 037/2016) and Cama- Mato-Grosso ao Amazonas, Anexo N° 5:1–49 + 1–3, 25 pls. rgo Correa Farm for the access authorization and Manoel Orsini, V. S., Nunes, A. V., Marsh, L. K. 2019. New dis- Teixeira for support. Adrian A. Barnett helped with the tribution records of Pithecia rylandsi and Pithecia mitter- English. meieri (Primates, Pitheciidae) and an updated distribu- tion map. Check List. 13(3). doi.org/10.15560/13.3.2123 Almério Câmara Gusmão, Programa de Pós-Graduação Peres, C. A. 1999. General guidelines for standardizing em rede Bionorte, Centro de Pesquisa em Limnologia, line-transect surveys of tropical forest primates. Neotrop. Biodiversidade e Etnobiologia do Pantanal, Cáceres, Bra- Primates 7: 11–16. zil, Universidade do Estado de Mato Grosso – UNEMAT. RADAMBRASIL. 1978. Projeto RADAMBRASIL. Vol. Av. Santos Dumont s/n° Cidade Universitária (Bloco II) (1-34). Geologia, geomorfologia, pedologia, vegetação e Cáceres – MT CEP 78.200-000, e-mail:
References PREDATION BY A SLATE-COLORED HAWK, LEUCOPTERNIS SCHISTACEA, ON JUVENILE Alvares, C. A., Stape, J. L., Sentelhas, P. C., Gonçalves, J. GRAELL’S BLACK MANTLED TAMARINS, LEON- L. M., Sparovek, G. 2014. Köppen’s climate classification TOCEBUS NIGRICOLLIS GRAELLSI map for Brazil. Meteorol. Zeitschrift. 22: 711–728. Cavalcante, T., Gusmão, A. C., Ferrari, S. F. 2018. Un- Josué Picho-Paucar expected diversity: the potential role of privately-owned Stella de la Torre forest remnants in the conservation of the primates of the highly-impacted Rondônia center of endemism, south- Introduction western Brazilian Amazonia. Neotrop. Primates 24(2): 82–85. Predation is considered an important factor in callitrichid De Lázari, P. R., Gusmão, A. C., Santos Filho, M., ecology and evolution (Caine 1993; Pulliam 1984). How- Casagrande, A. 2014. Extensão da distribuição geográfica ever, predation events on wild groups are difficult to -ob de Pithecia irrorata (Gray, 1842) para o sudoeste do Esta- serve (Ferrari 2009). Here we report two predation events do de Mato Grosso, Brasil. In: VIII Congresso Brasileiro de by the slate-colored hawk Leucopternis schistacea on one Mastozoologia, 2014, Gramado, PR. group of Graell’s black mantled tamarins Leontocebus nigri- Gusmão, A.C. Santos-Filho, M. 2015. Ocorrência de collis graellsi in Amazonian Ecuador. parauacú Pithecia cf. mittermeieri Marsh, 2014 (Pri- mates, Platyrrhini) na transição entre os biomas Panta- Study site nal, Amazônia e Cerrado, Mato Grosso, Brasil. Neotrop. Primates 22(1): 47–49. The predation eventstook place in Sacha Lodge Reserve, a Gusmão, A.C., Crispim, M. A., Ferronato, M. L. & Silva private area of well-preserved forest in the northern bank Júnior, J. S. 2014. Primatas da Reserva Particular do Pat- of the Napo River in Amazonian Ecuador (0°28’16.55” S, rimônio Natural (RPPN) Água Boa, Cacoal, Rondônia, 76°27’32.38” W). A group of seven Graell’s black mantled Brasil. Neotrop. Primates 21(2): 207–209. tamarins, Leontocebus nigricollis graellsi (2 adults, 24-26 cm; Hershkovitz, P. 1987. The taxonomy of South American 3 subadults, 22-23 cm; and 2 juveniles that were probably Sakis, genus Pithecia (Cebidae, Platyrrhini): A prelimi- twins (14-15 cm)), was followed from May 30 through Au- nary report and critical review with the description of a gust 9, 2018, to collect data of their feeding behavior. new species and a new subspecies. Am. J. Primatol. 12: 387–468. Results and Discussion Marsh, L. K. 2014. A taxonomic revision of the saki mon- keys, Pithecia Desmarest, 1804. Neotrop. Primates 21: On June 23, 2018, at 11:55 (local time), the tamarins were 1–163. feeding on Parkia sp. exudates and resting at about 25 m above ground. One of the individuals suddenly started to 76 Neotropical Primates 26(1), September 2020 emit alarm calls after a slate-colored hawk captured one of On August 4, 2018 at 9:35 we observed a second preda- the juveniles that was resting in the treetop of a Cecropia sp. tion event by a slate-colored hawk on the same tamarin The rest of group moved quickly to the treetop where the group. The six tamarins were resting ina kapok tree (Ceiba tamarin was caught, emitting alarm calls and apparently pentandra) at about 20 m above ground. The hawk caught trying to mob the hawk, but it flew to a nearby tree, hold- and squeezed the remaining juvenile with its claws while ing the juvenile in its claws (Fig. 1a and b). Once perched, the tamarin emitted distress calls. The hawk flew into the with its right claw the hawk grabbed the upper part of the forest while the rest of the tamarins began to move quickly tamarin, while using its beak to tear off the skin, moving emitting alarm calls. its head from side to side. At that moment, the rest of the tamarins moved back and hid in other trees. Twenty-two About 30 minutes after the predation event, the tamarins minutes after the hunt, the hawk left with the carcass. The were silent and vigilant, moving very slowly to an area about tamarins remained vigilant, producing sporadic alarm 600 m away. By late afternoon, the tamarins remained hid- calls. About 30 minutes after the hawk left, the tamarins den and quiet in the dense vegetation of the treetops until started moving very slowly and silently. They moved to an nightfall. The next day the tamarins were quiet, emitting area 500 m away from the hunting scenario, resting for 45 only very few alarm calls. They rested hidden the whole minutes on a tree about 30 m high. Late in the afternoon, morning and only moved in the afternoon. Three days lat- hours after the hunt, the group continued to be alert; they er, the group returned to their normal daily travel pattern. were difficult to follow, moving rapidly and quietly. At dusk the group remained together in a tree. The next These two successful predation events carried out in less day, June 24, the group started moving early, at around than two months point to the importance of the slate-color- 6:03 am, emitting very few vocalizations. The group trav- ed hawk in controlling this tamarin population. This spe- eled quickly through the forest all day, with a path length cies was reported hunting saddle-back tamarins in Peru that day of 875 m. Two days after the hunt, the tamarins (Lledo-Ferrer et al., 2009) but, to our knowledge, ours is seemed to return to their normal behavior, emitting more the first report of effective attacks of this raptor on Graell’s vocalizations and reducing their daily path to 750 m (daily black-mantled tamarins. It is remarkable that in both oc- paths were measured with ArcMap software using the GPS casions, the hawk hunted a juvenile, suggesting that it may coordinates recorded every time the group moved). use specific criteria to select its prey while observing tama- rin groups before the attack. The responseof this tamarin group to a predation event, moving faster, hiding and emit- ting fewer vocalizations in the next three to four days after the attack, is similar to that reported by Lledo-Ferrer et al. (2009) for saddle-back tamarins in Peru. This consistent response points to the strong influencethat predation pres- sure may have on tamarins’ behavior.
Acknowledgments
To Sacha Lodge, especially Guillermo Zaldumbide and An- drés Bustamante, as well as to all the staff, for their support to carry out this field research. To María Paula Ramírez for her assistance in the field, and to Rosa María Elvira Paucar and Juan Carlos Picho for their unconditional support and selfless help. To USFQ COCIBA Grants for research for partially funding the travel costs to the reserve.
Josué Picho-Paucar and Stella de la Torre, Universidad San Francisco de Quito, Colegio de Ciencias Biológicas y Ambientales.
References
Pulliam H. R. and Caraco T. 1984. Living in groups: Is there an optimal group size. In: Behavioural Ecology: An Evolutionary Approach. 2nd Ed. J.R. Krebs, N. B. Davies (eds.), pp. 122–147. Sinauer Associates, Sunderland. Figure 1. Slate-colored hawk Leucopternis schistacea feeding on Caine, N. G. 1993. Flexibility and co-operation as unifying a juvenile Graell’s black mantled tamarin Leontocebus nigricollis themes in Saguinus social organization and behaviour: the graellsi in Sacha Lodge Reserve, Amazonian Ecuador. role of predation pressures. In: Marmosets and tamarins: Neotropical Primates 26(1), September 2020 77
systematics, behaviour, and ecology, A. B. Rylands (ed.), Wright 1989; Donati and Borgognini-Tarli 2006; Fernan- pp. 200–219. Oxford University Press, Oxford. dez-Duque and Erkert 2006; Erkert et al. 2012; Khimji Ferrari, S. F. 2009. Predation risk and antipredator strategies. and Donati 2014). Nocturnal and diurnal activity in Aotus In: South American primates. Comparative perspectives in the spp. is influenced by moon luminosity and ambient tem- study of behavior, ecology, and conservation, P. A. Garber, A. perature (Fernandez-Duque 2003; Fernandez-Duque and Estrada, J. C. Bicca-Marques, E. W. Heymann, K. B. Strier Erkert 2006). The paucity of field studies on most Aotus (eds.), pp. 251–277. Springer, New York. species means that many aspects of their behavioral ecology Lledo-Ferrer, Y., Hidalgo, A., Heymann, E. W. and Peláez, are still unknown, and diurnal activity may be more com- F. 2009. Field observation of predation of a slate-color- mon than thought. ed hawk, Leucopternis schistacea, on a juvenile saddle-back tamarin, Saguinus fuscicollis. Neotrop. Primates 16(2): 82–84. The Peruvian night monkey (Aotus miconax) is one of the least studied of all Neotropical primates. This species is endemic to northern Peru (Shanee et al. 2015) and restrict- OBSERVATIONS OF DIURNAL ACTIVITY IN A ed to montane and pre-montane forests between ~1,200 ‘STRICTLY’ NOCTURNAL PRIMATE, THE PE- and 3,100 m a.s.l. (Shanee et al. 2015). This species is RUVIAN NIGHT MONKEY (AOTUS MICONAX), considered Endangered by the IUCN (2019). Aotus mi- YAMBRASBAMBA, PERU conax is considered a ‘strictly’ nocturnal night monkey (Fernandez-Duque 2011) and previously had only been Sam Shanee observed leaving and arriving at its nest sites between sun- Dan Doolan set and sunrise (Shanee et al. 2013). The diet ofA . miconax Nestor Allgas is highly omnivorous, composed of large amounts of ripe Claudia Salazar fruits, leaves and insects, and smaller amounts of buds and Vinciane Fack flowers (Shanee et al. 2013). Two studies have suggested the possibility of diurnal activity in A. miconax (Shanee et Introduction al. 2013; Campbell et al. 2019), but these studies did not document diurnal activities first hand. Cathemerality, definedas “sporadically active throughout a 24-hour day” (Fleagle 1988, p.52), or as “when significant Here we present ad libitum observations of diurnal behav- amounts of activity, particularly feeding and/or traveling, ior in Aotus miconax gathered in 2012 and 2018. The first occur within both the light and dark portions of that cycle” observations, from 2012, were made whilst surveying forest (Tattersall 1987, p. 201), is widespread across many mam- fragments in preparation for presence/absence surveys of mal species, in all major biomes (Curtis and Rasmussen A. miconax, and the 2018 observations, during behavioral 2006). As with nocturnality, cathemerality must confer studies of Lagothrix flavicauda, in continuous forest. As an evolutionary advantage. This advantage may be in the cathemerality in A. azarae and A. nigriceps is influenced by form of decreased interspecific competition, coping with light and temperature, we tested whether moon illumina- deficits in ambient light and temperature, and/or predator tion, moon phase, or ambient temperature had an effect on avoidance or prey capture (Curtis and Rasmussen 2006). instances of diurnal behavior in A. miconax.
It is probable that modern primates are descended from Study site and Methods nocturnal basal taxa (Ross et al. 2007; Santini et al. 2015). In the extant primates, nocturnal behavior is well estab- Observations were made at the El Toro field site, in Amazo- lished in the lorises and galagos, as well as several genera of nas region, Peru (05°39′46′′ S, 77°54′32′′ W) (Fig. 1), an lemur (Colquhoun 2011), and cathemerality is known in area of made up of ca. 700 ha of disturbed primary forest two genera of lemurs, Eulemur and Hapalemur (Colquhoun and regenerating secondary forest, interspersed with pas- 2011). There are also several published records of noctur- ture, that is part of continuous forest leading to the Amazo- nal behavior in other diurnal primate species including nian lowlands. Terrain in the area is very rugged, with high Cebus capucinus, Lemur catta, Macaca fuscata yakui, Pan ridges and deep valleys between 1,800 and 2,400 m a.s.l. troglodytes, and Rhinopithecus brelichi (Nishikawa and Mo- Annual rainfall is ca. 1,700 mm, with a drier season from chida 2010; Parga 2011; Perry 2012; Donati et al. 2013; August to December. The primary premontane and mon- Tan et al. 2013; Krief et al. 2014). tane forests of the area have been selectively logged over the past ~ 30 years and have a thick mid- and understory with Night monkeys (Aotus spp.) are the only nocturnal hap- an average canopy height of 15–25 m. The land is titled to lorhine, and subsequently the only nocturnal platyrrhines the Campesino Community of Yambrasbamba, with a single (Fernandez-Duque 2011). Most Aotus are considered land title of 80,545 ha. People in the community are pre- ‘strictly’ nocturnal, with only two species (A. azarae and A. dominantly subsistence farmers (tubers, corn and beans), nigriceps), in the southernmost, most seasonal, part of the with some small-scale commercial production (cattle, cof- genus distribution, showing cathemerality (Mann 1956; fee and ‘rocoto’). 78 Neotropical Primates 26(1), September 2020
conversation, generally people sought us out as they knew of our interest in local primates. These reports occurred sporadically during the entire period (2012-2018); we did not note the specific date of each report.
Results
We observed diurnal activity in Aotus miconax on 13 oc- casions during field work in 2012 (three observations) and 2018 (10 observations). All records were of ad libi- tum encounters either during behavioral follows of Lago- thrix flavicauda in continuous forest, during preparatory field work or during surveys of forest patches. Moon il- lumination on the nights preceding observations varied considerably (Table 1), between 10 % and 99 % (mean 43.09, ± 34.91), and showed no discernible trend (One sample Kolmogrov-Smirnov Test, 0.096). Average tem- peratures during the months of March to June 2018 were 19.6 °C during the day, and 11.5°C at night. There was no significant difference across the study period between diurnal and nocturnal temperatures when diurnal behav- iour was and was not observed (T-Test, t = 0.472, df = 242, p = 0.637). There was no significant difference from aver- age daytime temperatures on days when we observed A. miconax active during daylight hours (T-Test, t = 0.168, Figure 1. Map showing location of field site and surrounding df p villages. = 120, = 0.867). There was no significant difference from average nightime temperatures on nights immedi- ately preceding days when we observed A. miconax ac- Field trips for behavioral data collection on Lagothrix flav- tive during daylight hours (T-Test, t = 1.276, df = 120, icauda were carried out continuously from 2008 to 2019. p = 0.204). Trips were made every two weeks and lasted five days. Re- searchers left the field station at ~06:00 h each day and re- Table 1. Moon phases of the previous night, before diurnal turned at ~19:00 h each day during field trips. dditionalA observations. nocturnal surveys of Aotus miconax were made between March and June 2018 (Doolan 2018). All data collection Date of Moon illumination Moon phase was made by at least one researcher accompanied by expe- observation (% of full moon) rienced local field guides. Researchers carried standard field 27/1/12 23 % Waxing equipment; handheld GPS units were used to georeference 15/2/12 49 % Waning primate sightings and observations were aided by the use of binoculars and cameras with telephoto lenses. Obser- 26/2/12 26 % Waxing vations of Aotus diurnal activity were made during 2012 2/3/18 99 % Full moon and 2018. 25/3/18 54 % First quarter
We used moon illumination and phase data given in our 17/4/18 10 % Waxing handheld GPS units. We used ambient temperature data 17/5/18* 13 % Waxing for 2018 gathered on site (Lacrosse ws1600). As we only 30/5/18* 99 % Full moon collected weather data during our standard fieldwork we did not have a complete set for the entire period (March 12/6/18 11 % New moon – June 2018). When data were missing we used records 25/6/18 77 % Waxing from the Servicio Nacional de Meteorología e Hidrología del * Two separate observations on the same day Perú weather station at Chachapoyas (https://senamhi.gob. pe/?&p=estaciones). This station is the closest to the field Ad libitum observations from 2012 site (~ 60 km south), that is at a similar elevation (2,400 On the morning of the 28th of January 2012, during m a.s.l.). No temperature data were available for 2012, field surveys ofLagothrix flavicauda in continuous forest, so these observations were not included in hypothesis test- one unknown adult Aotus miconax individual, and three ing. We also recorded instances of diurnal behavior report- individuals (two adults and one juvenile) from a known ed to us by local informants and field guides. These -re group of A. miconax, were observed locomoting through ports consisted of information volunteered during normal the forest within the vicinity of the known group’s habitual Neotropical Primates 26(1), September 2020 79 sleeping site in a vine tangle in the lower crown, approx. 8 at 09:25 h during follows of Lagothrix flavicauda. The L. meters high, of a Ficus sp. tree. The observation took place flavicauda group was causing much disturbance, jumping at approximately 09:00 h. through the canopy and vocalizing, during this observation and probably disturbed the A. miconax group, although no On the 16th of February 2012, in a small patch of sec- direct interaction between the species was observed. ondary forest, ~1.4 ha (Shanee et al. 2013), just above the village of La Esperanza, two adult Aotus miconax individu- Additional observations als were observed feeding on ‘naranjillo’ (Styloceras laurifo- During presence/absence surveys and habitat characteri- lium) fruits. The observation took place at approximately zation of Aotus miconax in forest patches and continuous at 09:00 h. forest in 2018 (Doolan 2018), we inferred diurnal behavior on five occasions when we left groups at a nest site in the On the 27th of February 2012, in a small forest patch, < morning and did not find them there in the afternoon, or 1 h, just below the village of La Esperanza three Aotus mi- vice versa, when a group did not return to a particular nest conax individuals (two adults and one juvenile) were ob- in the morning but, was found there before sunset. Other served feeding on fruits in a fig tree (Ficus sp.). The obser- observations during this study included pairs of A. miconax vation took place at approximately 16:00 h. seen locomoting at ~10 a.m., but most probably this was due to disturbance by dogs in the area (Doolan, pers. obs). Ad libitum observations from 2018 On several other occasions, groups left their nests before On the 3rd of March 2018, we encountered a known group sunset or did not return until after sunrise, but these ob- of three Aotus miconax (two adults and one juvenile) that servations occurred within an hour of sunset or sunrise. A live close to the field station, awake and out of their nest. number of residents of the villages of La Esperanza, Mira- The group then travelled to a nearby tree where they fed on flores, and Santa Rosa (Fig. 1) have recounted observations figs (Ficus sp.). The observation took place at 13:06 h. On of A. miconax active during daylight hours whilst passing the 26th of March 2018 two members of the same Aotus through fragmented habitats to get to their fields. These miconax group (one adult and one juvenile) were again seen anecdotal reports cover the entire study period as well as active during the day, this time traveling through the trees. years preceding the start of our investigations. This observation took placeat 12:34 h. Discussion On the 18th of April 2018, again, two members of the same Aotus miconax group (one adult and one juvenile) Our observations show that, although classed as a ‘strictly were observed traveling through the trees. This observation nocturnal’ night monkey species, Aotus miconax is also ac- took place at 09:46 h. tive diurnally on occasion. This activity appears to be spo- radic and rare and is likely not enough to class it as cathem- On the 18th of May 2018, we observed two different eral to the same degree as A. a. azarai (Fernandez-Duque groups of Aotus miconax, one of four members (three adults 2003; Fernandez-Duque and Erkert 2006). Although and one juvenile) and two members (both adults), travel- field trips occurred during the intervening period, we did ling through the trees. Both observations took place at ap- not observe any diurnal A. miconax behavior during these proximately 10:4 h but, were recorded by different groups years. It is possible that diurnal activity in A. miconax was of observers simultaneously at different pointsof the field less frequent during these years, although local residents site. On the 31st of May 2018, we again observed two in- still reported instances to us. It is more probable that these stances of differentAotus miconax groups travelling during behaviors occurred at the same frequency, they were just the day time. The two groups (two adults, and two adults not noticed by ourselves or other researchers, particularly and a dependent infant, respectively) were seen at 08:49 h as we were not carrying out other investigations on A. mi- and 16:22 h, by different groups of observers in different conax during these periods. areas of the field site. The presence of a group of Lagothrix flavicauda passing through the area could have disturbed This is not the first report of Aotus miconax being active the A. miconax groups on these occasions, but no obvious during daylight hours. For example, Campbell et al. interactions were observed, and the A. miconax groups had (2019) recorded a group leaving their nesting site during still not returned to their nests for over 10 minutes after the daylight hours. Similarly, diurnal activity was inferred by L. flavicauda group had passed. Shanee et al (2013) when leaving groups at nesting sites in the morning, then findingthe sites empty prior to starting On the 13th of June 2018, three Aotus miconax individ- evening observations later the same day. However, in nei- uals (two adults and one juvenile) were seen travelling at ther of these studies were the animals observed feeding or 14:23 ha. Again, this was possibly due to disturbance by a traveling during daylight hours. Here we present many di- Lagothrix flavicauda group in the area. The group did not rect observations, showing that diurnal behaviors are more return to its nest or enter a new one for the 16 minutes of common than previously thought. our observations. On the 26th of June 2018 an unknown group of three Aotus miconax was found out of their nest 80 Neotropical Primates 26(1), September 2020
Nocturnal and diurnal activity in Aotus spp. is influenced moving through the trees in the Pacaya Samiria National by moon luminosity (Fernandez-Duque 2003; Fernan- Reserve at approximately 11:00 h. In both cases the groups dez-Duque and Erkert 2006). A. azarai azarai in the had disturbed by the activities of other primates, in these Argentinian Chaco show marked periodicity in their ac- cases Plecturocebus brunneus and Sapajus macrocephalus, re- tivity rhythms, being active throughout the night during spectively (N. Allgas, pers obs). Domestic animals have full moon nights, and displaying much less cathemerality also been observed to cause diurnal activity in A. miconax, (Fernandez-Duque 2003; Erkert 2004; Fernandez-Duque where individuals remain in or near human settlements af- and Erkert 2006). Our observations did not show any ter dawn, drawing the attention of dogs (Shanee and Sha- correlation of moon luminosity with diurnal behavior in nee 2011). It is also possible that at least some of these A. miconax, with animals seen active during the day light observations were due to unintentional disturbance by ob- hours on days preceded by anywhere between 11 and 99 % servers, or other human activity in the area. However, this illumination (Table 1). likely was not true in all cases, as on several occasions the animals were already engaged in other activities and away Temperature also has been linked to changes in nocturnal from their nesting sites before our arrival, and there were and diurnal activity in Aotus spp. (Erkert 1991; Fernan- no other humans in the vicinity. dez-Duque 2003; Fernandez-Duque and Erkert 2006). Temperatures on the nights preceding, and the days when The forests of Northern Peru suffer massive deforestation A. miconax were active in 2018 were not significantly dif- for agriculture, cattle ranching and timber extraction (IBC ferent to averages across the period (Fig. 2). Seasonal 2016). Deforestation has caused the fragmentation of changes in temperature, rainfall, and resource availability much of the remaining habitat of Aotus miconax, and most have not been found to influence occurrences of diurnal remaining habitat is disturbed (Shanee et al. 2015). Spe- behavior in A. azarae (Fernandez-Duque and Erkert 2006; cies that persist in heavily disturbed forests often develop Erkert et al. 2012). At our study site, just 5° south of the new ecological strategies to enable them to survive (Shanee equator, temperatures are fairly steady throughout the year. and Shanee 2011; Marsh et al. 2013), with those that are There are seasonal shifts in rainfall and resource produc- successful showing a high degree of behavioral and dietary tion, although our limited data set preclude possibilities of plasticity (Castano et al. 2010; Shanee and Shanee 2011; testing the influence of seasonality. Interestingly, sympat- Marsh et al. 2013). ric Lagothrix flavicauda groups at the study site have been Very few observations of diurnal activity have been report- ed for Aotus spp. (Mann 1956; Khimji and Donati 2014) other than A. a. azarai (Fernandez-Duque 2003; Fernan- dez-Duque and Erkert 2006), and this behavior has only previously been inferred for A. miconax on a handful of occasions (Shanee et al. 2013; Campbell et al. 2019). As with most species of Aotus, detailed studies of all aspects of A. miconax behavioral ecology are lacking. It is very pos- sible that further observations of this species will indicate that diurnal activity is more common than thought.
Acknowledgments noted to significantly change their activity budgets and di- ets between seasons (Fack et al. submitted). We wish to thank the people and authorities of Yam- brasbamba, the Mego and Gonzales families, Wilder Figure 2. Average monthly diurnal and nocturnal temperatures on days and nights, immediately preceding, observations of diur- Chuquitucto, Pascual Diaz, and Wilder Gonzalez. We nal activity in Aotus miconax in 2018. also thank the various volunteers who accompanied us. Funding for this research came from the Fonds Nation- Some of our observations occurred through disturbance al de La Recherche Scientifique, Fonds Léopold III pour of the night monkeys by other animals. Nocturnal activity l’Exploration et la Conservation de la Nature, and Neo- in several species of diurnal primate have been observed tropical Primate Conservation, through grants from the (Nishikawa and Mochida 2010; Parga 2011; Donati et al. International Primate Protection League, Primate Society 2013; Tan et al. 2013; Krief et al. 2014), in some cases of Great Britain, American Society of Primatologists, Wild provoked by the activity of nocturnal species (Nishikawa futures, and Primate Conservation Inc. Research was con- and Mochida 2010; Krief et al. 2014). During our surveys, ducted under permits 029-2012-AG-DGFFS-DGEFFS Aotus miconax were disturbed from their nests by Lagothrix and 350-2017-SERFOR/DGGSPFFS. flavicauda on a number of occasions. Similarly, a group of four A. nigriceps was observed locomoting between 09:30 Sam Shanee, Neotropical Primate Conservation, Win- and 10:00 h at Tambopata National Reserve, in South- drush, Looe Hill, Seaton, Cornwall, UK; Asociacion Ne- ern Peru, and another group of A. nancymaae, observed otropical Primate Conservation Perú, Villa El Salvador, Neotropical Primates 26(1), September 2020 81
Lima, Peru, e-mail:
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Into the night: Venezuela – Lizarralde, M.; 7) Memories, monkeys and the camera traps reveal nocturnal activity in a presumptive Mapoyo people: Rethinking ethnoprimatology in eco-his- diurnal primate, Rhinopithecus brelichi. Primates. 54: 1-6. torical contexts of the middle Orinoco, Venezuela – Urba- Tattersall, I. 1987. Cathemeral activity in primates: A defi- ni, B.; 8) Co-ecology of Jotï, primates, and other people: nition. Folia Primatol. 49: 200-202. A multispecies ethnography in the Venezuelan Guayana – Wright, P. C. 1989. The nocturnal primate niche in the Zent, S., et al.; 9) Primates in the lives of the Yanomami New World. J. Hum. Evol. 18: 635-658. people of Brazil and Venezuela – Boubli, J. P., et al.; 10) Kixiri and the origin of day and night: Ethnoprimatology among Waimiri Atroari Ameindians of the Central Ama- zonia, Brazil - Souza Mazurek, R. R., et al.; 11) Linguistic, Recent Publications cultural and environmental aspects of ethnoprimatological knowledge among the Lokono, Kari’na and Warao of the Moruca river (Guyana) – Rybka, K.; 12) Relationships be- tween scientific ecology and knowledge of primate ecology BOOKS of Wapishana subsistence hunters in Guyana – Henfrey, T.; 13) Past, present and future of Secoya ethnoprimatology in Skeletal Anatomy of the Newborn Primate, by Smith, T. D, the Ecuadorian Amazonia – Torre, S., et al.; 14) The im- DeLeon, V. B., Vinyard, C. J. and Young, J. W. Cambridge portance of nonhuman primates in Waorani communities University Press, 328pp. 2020. ISBN: 978-1107152694. of the Ecuadorian Amazon – Levin, M. F.; 15)Monkeys in This is the first book dedicated to newborn skeletal and the Wampis (Huambisa) life and cosmology in the Peruvian dental anatomy and how it varies across primate species. Amazonian rainforest – Swierk, K.; 16) The white monkey Structured according to anatomical regions, the book and the Pelejo monkey: Primates in the social and cultural includes hundreds of detailed anatomical illustrations, configurations of the Shawi people of Northwestern Peru including a color atlas illustrating entire skeletons in rep- - Gonzalez Saavedra, L.; 17) The importance of primates resentative taxa. Whilst the book is primarily a guide to to Tacaba indigenous subsistence hunting on the Bolivian comparative anatomy, it also highlights the links between Amazon – Townsend, W. R., et al; 18) When monkeys were development and behavior. Content: 1) Introduction; 2) humans: Narratives of the relationship between primates Primate development and growth; 3) Why ontogeny mat- and the Qom (Toba) people of the Gran Chaco of Argenti- ters; 4) The skull; 5) Dentition; 6) The postcranial axial na – Medrano, C., et al. skeleton; 7) The pectoral girdle and forelimb skeleton; 8) The pelvic girdle and hindlimb skeleton; 9) The newborn New World Monkeys: The Evolutionary Odyssey, by Rosen- primate body form: phylogenetic and life history influenc- berg AL. Princeton University Press, 368pp. 2020. ISBN: es; 10) Ontogeny of feeding; 11) Ontogeny of locomotion. 978-0691143644. Based on the most current findings, this book offers the first synthesis ofdecades of fieldwork and Neotropical Ethnoprimatology: Indigenous Peoples’ Perceptions laboratory and museum research conducted by hundreds of and Interactions with Nonhuman Primates (Ethnobiology), of scientists on evolution of New world primates. Content: edited by Urbani, B. and Lizarralde, M. Springer, 427pp. 1) What is a New world monkey? 2) Diverse lifestyles; 3) 2020. ISBN: 978-3030275037. This book reviews the What’s in a name? 4) Evolutionary models; 5) How to eat complex interconnections between different indigenous like a monkey; 6) Arboreal acrobats; 7) Many kinds of peoples with New World monkeys that sympatrically share Platyrrhine brains; 8) The varieties and means of social or- their ancestral territories. It includes study cases in a geo- ganization; 9) 20 million years: every fossil tells a story; 10) graphic range that covers all of the Neotropics, from south- South America was once and island: how did Platyrrhine ern Mexico through northern Argentina. Contents: 1) Per- ancestors get there? 11) After 20 million years of existence, ceptions and uses of primates among Popoluca indigenous New world monkeys face extinction. people in Los Tuxtlas, Mexico - Pinto Marroquin, M., et al.; 2) Mental state attribution to nonhuman primates and other animals by rural inhabitants of the community of Conhuas ARTICLES near the Calakmul Biosphere Reserve in the Yucatan Penin- sula Mexico - Urquiza-Haas, E. G., et al.; 3) Local knowl- Adams, D. B., Kitchen, D. M. 2020. Model vs. play- edge and cultural significance of primates (Ateles geoffroyi back experiments: The impact of sensory mode on and Alouatta pigra) among Lacandon Maya from Chiapas, Neotropical Primates 26(1), September 2020 83
predator‐specific escape responsesin saki monkeys. Ethol- del Toro, C. J., Mondragón-Ceballos, R. and Gutiér- ogy, 126(5): 563–575. rez-García, G. 2020. Potential food availability influences Arakaki, P. R., de Agostini Losano, J. D., Salgado, P. A. B. social interactions of young Individuals in a Neotropical and Pereira, R. J. G. 2020. Seasonal effects on testes size primate (Alouatta palliata). Folia Primatol. 91(1): 31–47. and sustained semen quality in captive golden-headed De Marco, A., Cozzolino, R. and Thierry, B. 2020. Re- lion tamarins, Leontopithecus chrysomelas. Anim. Reprod. sponses to a dead companion in a captive group of tufted Sci. 106472 capuchins (Sapajus apella). Primates 61(1): 111–117. Aximoff, I., Zaluar, M. .,T Pissinatti, A., Bastos, P. A., de Dias, P. A., Montero Domínguez, I. L. and Rangel Negrín, Assis Morais, T., da Rosa, C. A., et al. 2020. Anomalous A. 2020. Factors influencing infant sex ratio in howler Pigmentation in Invasive and Native Marmosets, Cal- monkeys (Alouatta spp.): A literature review and analysis. lithrix jacchus, Callithrix penicillata (Primates, Callitrichi- Am. J. Phys. Anthropol. 172(1): 48–57. dae), and Their Hybrids in Brazil.Folia Primatol. 91(2): Dolotovskaya, S. and Heymann, E.W. 2020. Do less or eat 149–158. more: strategies to cope with costs of parental care in a Berthaume, M.A., Lazzari, V., Guy, F. 2020. The landscape pair-living monkey. Anim. Behav. 163: 163–173. of tooth shape: Over 20 years of dental topography in Fack, V., Shanee, S., Drubbel, R. V., Meunier, H. and primates. Evol. Anthropol. 1–18 Vercauteren, M. 2020. Geophagy in Wild Yellow-Tailed Bucher, B., Bourgeois, M., Anderson, J.R., Kuroshima, H., Woolly Monkeys (Lagothrix flavicauda) Is Brief and Rare. Fujita, K. 2020. Investigating reactions of squirrel mon- Int. J. Primatol. 41(4): 566–582. keys (Saimiri sciureus) towards unequal food distributions Fack, V., Shanee, S., Drubbel, R. V., Vercauteren, M. in a tray‑pulling paradigm. Primates 61: 717–727. and Meunier, H. 2020. Geophagy in the yellow-tailed Bwye, P. and Toyne, A. 2020. Hand-rearing protocol and woolly monkey (Lagothrix flavicauda) at La Esperanza, comparison of growth rates in parent reared versus hand Peru: site characterization and soil composition. Primates reared offspring: a case study inCallicebus cupreus. J. Zoo 61:507–518. Aquar. Res. 8(2): 146–151. Fergnani, D. M., Kowalewski, M. M. and Fernandez, Carducci, P., Squillace, V., Manzi, G. and Truppa, V. 2020. V.A. 2020. Germination of native and exotic seeds dis- Touch improves visual discrimination of object features persed by wild black-and-gold howler monkeys (Alouatta in capuchin monkeys (Sapajus spp.). Behav. Processes. caraya): assessing deinhibition and scarification effects. 172: 104044. Primates 61: 519–527 Carneiro, J., Sampaio, I., Lima, T., Silva‐Júnior, J. D. S., Fernandes, O. J., Porfirio, G. E. O., Santos, .M.,F Arruda, Farias, I., Hrbek, T., et al. 2020. Phylogenetic relation- W., Oliveira, W. et al. 2020. Behavioral activities and diet ships in the genus Cheracebus (Callicebinae, Pitheciidae). of Azaras’s capuchin monkey, Sapajus cay (Illiger, 1815), Am. J. Primatol. 82(9): e23167. in a forest remnant of the Brazilian Cerrado. Stud. Ne- Coimbra, D. P., Penedo, D. M., Silva, M. O., Abreu, A. otrop. Fauna E. 55(2): 149–154. P., Silva, C. B., Verona, C. E., et al. 2020. Molecular and Ferreguetti, A. C., Oliveira, A., Pereira, B. C., Santori, R. morphometric identification of Trypanosoma (Megatryp- T., Geise, L. and Bergallo, H. G. 2020. Encounter rate anum) minasense in blood samples of marmosets (Cal- and behavior of Alouatta guariba clamitans in the Ilha lithrix: Callithrichidae) from the city of Rio de Janeiro, Grande State Park, Rio de Janeiro state, Brazil. Zoologia Brazil. Parasitol. Int. 75: 101999. 37: e36846. Costa, T. S., Nogueira‐Filho, S. L., De Vleeschouwer, K. Garber, P. A., McKenney, A., Bartling-John, E., Bic- M., Oliveira, L. C., de Sousa, M. B. C., Mendl, M., et ca-Marques, J. C., De la Fuente, M. F., Abreu, F., et al. al. 2020. Individual behavioral differences and health of 2020. Life in a harsh environment: the effects of age, sex, golden‐headed lion tamarins (Leontopithecus chrysomelas). reproductive condition, and season on hair cortisol con- Am. J. Primatol. 82(5): e23118. centration in a wild non-human primate. PeerJ 8: e9365. de Almeida‐Rocha, J. M., Peres, C. A., Monsalvo, J. A. Garbino, G. S., da Silva, L. H., Amaral, R. G., Rezende, G. and Oliveira, L. D. C. 2020. Habitat determinants of C., Pereira, V. J., Culot, L. 2020. Predation of tree frogs golden‐headed lion tamarin (Leontopithecus chrysomelas) (Anura: Hylidae) with toxic skin secretions by the black occupancy of cacao agroforests: Gloomy conservation lion tamarin (Leontopithecus chrysopygus, Callitrichinae). prospects for management intensification.Am. J. Prima- Primates 61: 567–572. tol. 82: e23179. Gonçalves, F. B., Gonçalves, B. S., Cavalcante, J. S. and de la Chica, A. G., Huck, M., Depeine, C., Rotundo, M., Azevedo, C. V. 2020. Aging-related changes on social Adret, P., Fernandez-Duque, E. 2020. Sexual dimor- synchronization of circadian activity rhythm in a diurnal phism in the loud calls of Azara’s owl monkeys (Aotus primate (Callithrix jacchus). Chronobiol. Int. 1–13. azarae): evidence of sexual selection? Primates 61(2): Guerrero-Casado, J., Cedeño, R. I., Johnston, J. C. and 309–319. Gunther, M. S. 2020. New records of the critically en- del Rio, J., Aristide, L., dos Reis, S. F., dos Santos, T. 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Guimarães-Lopes, V. D. P., Gomes, M. R. V. S., Kag- and its Wolbachia from Red Howler Monkeys (Alouatta ueyama, M., Faria, R. D. C. V., Ribeiro Filho, O. P., de macconnelli) in French Guiana—A Preliminary Study. Melo, F. R. and Sartori, S. S. R. 2020. Anatomical pa- Pathogens 9(8): 626. rameters of the body and the digestive tract of Callithrix Landman, R., Sharma, J., Hyman, J. B., Fanucci-Kiss, A., sp. marmosets under the influence of seasonality. Anat Meisner, O., Parmar, S., ... and Desimone, R. (2020). Histol Embryol. 49: 511–520. Close-range vocal interaction in the common marmoset Hecht, E. E., Reilly, O. T., Benítez, M., Phillips, K. A. and (Callithrix jacchus). Plos One, 15(4): e0227392. Brosnan, S. 2020. Sex differences in the brains of capuchin Lau, A. R., Clink, D. J. and Bales, K. L. 2020. Individu- monkeys (Sapajus [Cebus] apella). J. Comp. Neurol. 1–13 ality in the vocalizations of infant and adult coppery titi Helenbrook, W. D., Nelson, A., Paras, K. 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A. and Rovirosa-Hernán- Acta Trop. 105534. dez, M. D. J. 2020. Nocturnal mother–juvenile offspring Melo‐Carrillo, A., Dunn, J.C., Cortés‐Ortiz, L. 2020. Low interaction at the beginning of the juvenile period in genetic diversity and limited genetic structure across the free-ranging spider monkeys (Ateles geoffroyi): a report on range of the critically endangered Mexican howler mon- two cases. Ethol. Ecol. Evol. 32(4): 374–388. key (Alouatta palliata mexicana). Am. J. Primatol. 82(8): Hodges, S. 2020. Observations of infant conflict and e23160. avoidance in San Martin titi monkeys (Plecturocebus oe- Mercier, F., Witczak, L. R. and Bales, K. L. 2020. Coppery nanthe). Primates 61: 365–371. titi monkey (Plecturocebus cupreus) pairs display coordi- Hodges, S. 2020. Observations of infant conflict and nated behaviors in response to a simulated intruder. Am. avoidance in San Martin titi monkeys (Plecturocebus oe- J. Primatol. 82: e23141. nanthe). Primates 61: 365–371. Monroy-Cendales, M. 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bias: Capuchin monkeys (Sapajus apella) prefer densely because they are dangerous? A test of the Risk Hypothesis arranged items in a food-choice task. J. Comp. Psychol. in white-faced capuchin monkeys (Cebus capucinus). Int. 134(2): 232–240. J. Primatol.41: 246–264 Presotto, A., Remillard, C., Spagnoletti, N., Salmi, R., Valeri, M. P., Dias, G. B., Moreira, C. N., Yonenaga-Yas- Verderane, M., Stafford, K., etal. 2020. Rare bearded suda, Y., Stanyon, R. and Svartman, M. 2020. Charac- capuchin (Sapajus libidinosus) tool-use culture is threat- terization of Satellite DNAs in Squirrel Monkeys genus ened by land use changes in northeastern Brazil. Int. J. Saimiri (Cebidae, Platyrrhini). Sci. Rep. 10(1): 1–11. Primatol. 41(4): 596–613. Van Belle, S. and Estrada, A. 2020. The influence of loud Runestad Connour, J., Glander, K. E. 2020. Sexual dimor- calls on intergroup spacing mechanism in black howler phism and growth in Alouatta palliata based on 20+ years monkeys (Alouatta pigra). Int. J. 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How ecological and social factors influence the timing of Rosso, J. R., Schreier, A. L., Coggeshall, E. M., Merrigan- natal dispersal. johnson, C. and Bolt, L. M. 2019. The influence of -an Ellis, K. M., Abondano, L. and Di Fiore, A. 2019. Flexible thropogenic forest edge on the social cohesion of mantled grouping patterns of lowland woolly monkeys (Lagothrix howler monkeys in Costa Rica. lagotricha poeppigii): evidence of a multilevel society in a Runestad Connour, J., Canington, S. L. and Nida, K. New World primate? 2109. Ateles species differences in limb bone properties, Fogaca, M. D., Laird, M. F., Wright, B. W., Salmi, R. and body length, and sexual dimorphism. Santos, R. R. 2019. To cook or not to cook: shellfish Rutherford, J., Ross, C., Layne Colon, D., Sills, A., Ziegler, feeding in tufted capuchins. T. and Tardif, S. 2019. What goes around: Mothers’ birth Halenar-Price, L. B., Shearer, B., Terhune, C. E., Yoakum, condition influences daughters’ age at first pregnancy and C. and Cooke, S. B. 2019. Get an eyeful of this: Gross uterine size in the common marmoset (Callithrix jacchus). anatomy and morphometrics of the squirrel monkey Scarry, C. J., Link, A. and Di Fiore, A. 2019. Sex differ- (Saimiri) interorbital region. ences in behavioral coordination in white-bellied spider Henriques Viscardi, L., Rodrigues Paixão-Côrtes, V., Re- monkeys. ales, G., Webster, T. H., Bortolini, M. and Guerra Amor- Siegel, N. D. and Vinyard, C. J. 2019. Trabecular ontogeny im, C. 2109. Male mutation bias is pervasive across of the mandibular condyle in callitrichids. primates. Veilleux, C. C., Hiramatsu, C., Webb, S., Aureli, F., Schaff- Herrera, B. and Hubbe, M. 2019. Correlations between ner, C. M., Kawamura, S. and Melin, A. D. 2019. I see, cranial morphometric variation and climate in western you smell: interspecific variation in sensory use for fruit South America. evaluation among sympatric New World monkeys. Hicks, H. N. 2019. Differences in grooming behaviors in Yoakum, C. B. and Terhune, C. E. 2019. An assessment mantled howler monkeys (Alouatta palliata) based on of the neurovascular structures of the trigeminal nerve weather conditions. and their relationship to tooth morphology in Rattus sp., Hodges, S. 2019. Paternal activity budgets of San Martin Pithecia pithecia, Saimiri sciureus, and Chiropotes sp. titi monkeys (Plecturocebus oenanthe) in response to hab- itat destruction, daily temperature range, and infant age. Hogan, J. D., Fedigan, L. M., Hiramatsu, C., Kawamu- ra, S. and Melin, A. D. 2019. Seeing the flowers for the Meetings trees: trichromacy provides food detection advantages for white-faced capuchins. Hores, R. M. and Ford, S. M. 2019. Diversity and distri- bution patterns of a primate community in the Peruvian AMERICAN ASSOCIATION OF PHYSICAL Amazon. ANTHROPOLOGISTS MEETING King-Bailey, G. L. Jack and K. M. 2019. Determining dominance rank order in wild female white-faced capu- The 90th AAPA annual meeting will be held inBaltimore, chins: a comparison of three methods. Maryland from April 7-10, 2021. For more information, Klukkert, Z. S. 2019. Functional correlates of jaw shape please visit physanth.org/meetings-and-webinars/90th-an- diversity in platyrrhine sclerocarpic harvesters. nual-meeting-7-10-april-2021-baltimore/ Ledogar, J. A., Wright, B. W., Granatosky, M. C., Laird, M. F., Chalk-Wilayto, J., Fogaça, M. D., Van Casteren, A., Ross, C. F. and Strait, D. S. 2019. Food mechanical IPS/SLAPRIM CONGRESS 2020 POSTPONED TO properties and dietary ecology in sympatric Pithecia and 2021 Chiropotes during a period of preferred food scarcity. Milich, K. M., Sorbello, K., Mccarten, J., Wiseman-Jones, Because of COVID-19 global situation the joint meet- L., Busobozi, R. and Kugonza, M. 2019. Conservation ing of the 28th IPS Congress and the IV Congress of the to coexist: Participatory action research for wildlife con- SLAPRIM will be postponed to August 15 – 21st, 2021 servation, economic development, and biological anthro- in Quito, Ecuador. A “second-chance” registration period pology research. will be opened in early 2021 for anyone who is not cur- Milstein, M. S., Shaffer, C. .,A Wolf, T. M. and Travis, D. rently registered but would like to register and submit a A. 2019. An ethnographic approach to characterizing new abstract for the rescheduled meeting. For more infor- zoonotic disease risk from primate hunting in an indige- mation go to www.internationalprimatologicalsociety.org/ nous reserve in Guyana. announcements.cfm Poindexter, S. A., Decamp, R. M. and Garrett, E. C. 2019. Navigational demand and how it’s linked to olfaction and spatial memory in primates. INTERNATIONAL PRIMATOLOGICAL SOCIETY Porter, L. M. and Erb, W. M. 2019. Inter- and intra-group variation in infant transport in wild Weddell’s saddleback The 29th IPS Congress has been rescheduled to be 2 years tamarins (Leontocebus weddelli) in northwestern Bolivia. later, in 2023 in Kuching, Malaysia.
PRIMATES DE PERÚ GUÍA DE IDENTIFICACIÓN DE BOLSILLO
Authors: Rolando Aquino Y., Fanny M. Cornejo, Please complete the following form and mail or Liliana Cortés Ortiz, Filomeno Encarnación C., email to: Eckhard W. Heymann, Laura K. Marsh, Russell A. Jill Lucena Mittermeier, Anthony B. Rylands and Jan Vermeer. Global Wildlife Conservation Illustrated by Stephen D. Nash. $7.95. (price 718 7th Street NW includes UPS ground shipping to U.S. addresses) Washington, DC 20001 USA ISBN: 978-1-934151-91-4. First Edition. 2015. Tel (202) 369-1194 Email: [email protected] Also available in English.
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News items. Please send us information on projects, field Scope sites, courses, Thesis or Dissertations recently defended, recent publications, awards, events, activities of Primate Societies, etc. The journal aims to provide a basis for conservation information References. Examples of house style may be found throughout this relating to the primates of the Neotropics. We welcome texts on any journal. In-text citations should be first ordered chronologically and aspect of primate conservation, including articles, thesis abstracts, then in alphabetical order. For example, “…(Fritz, 1970; Albert, news items, recent events, recent publications, primatological society 1980, 2004; Oates, 1981; Roberts, 2000; Smith, 2000; Albert et al., information and suchlike. 2001)…”
Contributions In the list of references, the title of the article, name of the journal, and editorial should be written in the same language as they were Manuscripts may be in English, Spanish or Portuguese, should be published. All conjunctions and prepositions (i.e., “and”, “In”) should prepared with MS Word, and must use page and line numbering. The be written in the same language as rest of the manuscript (i.e., “y” or full name and address for each author should be included. “e”, “En” or “Em”). This also applies for other text in references (such Please avoid abbreviations and acronyms without the name in as “PhD thesis”, “accessed” – see below). Please refer to these examples full. Authors whose first language is not English should have their when listing references: manuscripts written in English carefully reviewed by a native speaker. Send all contributions to BOTH: Erwin Palacios, Conservacion Internacional – Colombia, e-mail: [email protected] and Journal article to Jessica Ward Lynch, University of California, Los Angeles, email: Stallings, J. D. and Mittermeier, R. A. 1983. The black-tailed [email protected]. Manuscripts that do not conform to the marmoset (Callithrix argentata melanura) recorded from Paraguay. Am. formal requirements (formatting, style of references, etc.) will be J. Primatol. 4: 159–163. returned to authors without review. They can be resubmitted, provided all formal requirements are met. Chapter in book Brockelman, W. Y. and Ali, R. 1987. Methods of surveying and Articles. Each issue of Neotropical Primates will include up to three sampling forest primate populations. In: Primate Conservation in full articles, limited to the following topics: Taxonomy, Systematics, the Tropical Rain Forest, C. W. Marsh and R. A. Mittermeier (eds.), Genetics (when relevant for systematics and conservation), Bioge- pp.23–62. Alan R. Liss, New York. ography, Ecology and Conservation. Text for full articles should be Book typewritten, double-spaced with no less than 12 cpi font (preferably Catalogue of Primates in the British Museum Times New Roman) and 3-cm margins throughout, and should not Napier, P. H. 1976. (Natural History) exceed 25 pages in length (including references). Please include an . Part 1: Families Callitrichidae and Cebidae. British abstract in the same language as the rest of the text (English, Spanish Museum (Natural History), London. or Portuguese) and (optional) one in Portuguese or Spanish (if the text Thesis/Dissertation is written in English) or English (if the text is written in Spanish or Wallace, R. B. 1998. The behavioural ecology of black spider monkeys Portuguese). Tables and illustrations should be limited to six, except in north-eastern Bolivia. Doctoral thesis, University of Liverpool, in cases where they are fundamental for the text (as in species descrip- Liverpool, UK. tions, for example). Full articles will be sent out for peer-review. For articles that include protein or nucleic acid sequences, authors must Report deposit data in a publicly available database such as GenBank/EMBL/ Muckenhirn, N. A., Mortensen, B. K., Vessey, S., Fraser, C. E. O. and DNA Data Bank of Japan, Brookhaven, or Swiss-Prot, and provide an Singh, B. 1975. Report on a primate survey in Guyana. Unpublished accession number for inclusion in the published paper. report, Pan American Health Organization, Washington, DC.
Short articles. These manuscripts are usually reviewed only by the Website editors. A broader range of topics is encouraged, including such as UNESCO. 2005. UNESCO Man and the Biosphere Programme. behavioral research, in the interests of informing on general research United Nations Educational, Scientific, and Cultural Organisation activities that contribute to our understanding of platyrrhines. We (UNESCO), Paris. Website: http://www.unesco.org/mab/index.htm. encourage reports on projects and conservation and research programs Accessed 25 April 2005. (“Acessada em 25 de abril de 2005” and (who, what, where, when, why, etc.) and most particularly information “Consultado el 25 de abril de 2005” for articles in Portuguese and on geographical distributions, locality records, and protected areas and Spanish respectively). the primates that occur in them. Text should be typewritten, double- spaced with no less than 12 cpi (preferably Times New Roman) font For references in Portuguese and Spanish: and 3-cm margins throughout, and should not exceed 12 pages in “and” changes to “e” and “y” for articles in Portuguese and Spanish length (including references). respectively. “In” changes to “Em” and “En” for articles in Portuguese and Spanish respectively. Figures and maps. Articles may include small black-and-white photographs, high-quality figures, and high-quality maps. “Doctoral thesis” changes to “Tese de Doutoramento” and “Tesis de (Resolution: 300 dpi. Column widths: one-column = 8-cm wide; Doctorado” for articles in Portuguese and Spanish respectively. two-columns = 17- cm wide). Please keep these to a minimum. We stress the importance of providing maps that are publishable. When “MSc Thesis” changes to “Dissertação de Mestrado” and “Tesis de reporting geographic coordinates please utilize one of the following Maestría” for articles in Portuguese and Spanish respectively. formats consistently throughout the manuscript: DMS (degrees, minutes, seconds) 4°’36’19.1’’N, 74°3’20.7’’W or DD (Decimal “Unpublished report” changes to “Relatório Técnico” and “Reporte Degrees) 4.605306, -74.055750. no publicado” for articles in Portuguese and Spanish respectively. Neotropical Primates A Journal and Newsletter of the IUCN/SSC Primate Specialist Group Vol. 26(1), September 2020 Contents
Articles Human-Monkey Interaction Dynamics and Their Dietary Impacts on Central American White-Faced Capuchins (Cebus imitator) at Manuel Antonio National Park, Costa Rica Meredith Schulte, Gustavo Gutiérrez-Espeleta and Jessica W. Lynch...... 1 Anti-Predator Behavior of Coimbra-Filho’s Titi Monkeys (Callicebus coimbrai) João Pedro Souza-Alves and Isadora P. Fontes...... 10 Not so Peaceful: Aggressive Encounters Between Beni Titi Monkey (Plecturocebus modestus) Groups in Bolivia Jesus Martinez, Pamela Carvajal and Robert Wallace...... 17 Unusual Behavioral Responses of the South American Coati (Nasua nasua) to the Hooded Capuchin (Sapajus cay) in the Paraguayan Upper Paraná Atlantic Forest Rebecca L. Smith, Emily Briggs and Paul Smith...... 23 Trends in the Use of Studbooks in Captive Breeding Programs of Neotropical Primates María Laura Muñoz-Lora, Kárem Gómez-Cadenas, Ana Carolina Falla and Iván Darío Soto-Calderón...... 30 Ocorrência, Ecologia e Conservação do Guigó-da-Caatinga (Callicebus barbarabrownae - Hershkovitz, 1990) Udemario Maia Ribeiro, José Monteiro do Nascimento Junior, Francisco Mário Fagundes Barbosa e Marcos Roberto Rossi dos Santos...... 41 Population Density Estimate for the White-Faced Capuchin Monkey (Cebus imitator) in the Multiple Use Area Montaña La Botija, Choluteca, Honduras, and A Range Extension for the Species Eduardo José Pinel Ramos...... 47 Reducción en la Densidad Poblacional del Titi Gris (Saguinus leucopus) en el Oriente de Caldas, Colombia Néstor Roncancio D., Jennifer Branch B., Oscar Felipe Moreno-Mancilla, María Isabel Blanco N., Oscar Ospina H. and Lina Marcela Guzmán...... 56
Short Articles Primate Densities at Río Puré National Park, Eastern Colombian Amazonia Erwin Palacios ...... 64 New Records of Brachyteles arachnoides (É. Geoffroy, 1806) (Primates: Atelidae) in the Southern Atlantic Forest, in Paraná State, Brazil Cláudia Golec Fialek, Mayara Cristina Gaspari, Tiago Luiz Daros, Maria Harumi Yoshioka and Sérgio Bazilio...... 69 Pithecia mittermeieri (Marsh, 2014) Geographic Distribution: New Records Extend the Range East of the Juruena River Almério Câmara Gusmão, Odair Diogo da Silva, Ana Lúcia Cardoso Martins, Vancleber Divino Silva Alves and Manoel dos Santos Filho...... 72 Predation by a Slate-Colored Hawk, Leucopternis schistacea, on Juvenile Graell’s Black Mantled Tamarins, Leontocebus nigricollis graellsi Josué Picho-Paucar and Stella de la Torre ...... 75 Observations of Diurnal Activity in a ‘Strictly’ Nocturnal Primate, the Peruvian Night Monkey (Aotus miconax), Yambrasbamba, Peru Sam Shanee, Dan Doolan, Nestor Allgas, Claudia Salazar and Vinciane Fack...... 77 Recent Publications...... 82
Meetings...... 86